Animal Models Used by PREVENT

Jump to:  Colon | Endometrium/ Uterus | Esophagus | Head and Neck | Liver | Lung | Mammary Gland | Mesothelioma | Other, Solid Tumors | Ovary | Pancreas | Prostate | Urinary Bladder

Organ Site High Risk Cohort Species (Strain) Method of Tumor Induction Endpoint(s) Measured Ref.
Colon Familial adenomatous polyposis (FAP) patients; Individuals at high risk for colorectal cancer (CRC) Mouse (C57BL/6J-ApcMin/+ or FVB) AOM Adenoma, adenocarcinoma [1,2]
Familial adenomatous polyposis (FAP) patients; Individuals at high risk for colorectal cancer (CRC) Rat (F344) AOM ± DSS ACF, adenoma, adenocarcinoma
[3-9]
Inflammatory bowel disease (IBD) patients at high risk for CRC (support pending) Mouse (BALB/c-IL-4-/-) AOM + TNBS Adenoma, adenocarcinoma
[10]
Familial adenomatous polyposis (FAP) patients Min mouse (ApcMin/+) Apc (germline mutation) Adenoma (small intestine)
[2,7,11-13]
Familial adenomatous polyposis (FAP) patients Min mouse (AKR/J-ApcMin/+) Apc (germline mutation) backcrossed with AKR mouse Adenoma, adenocarcinoma (colon, small intestine)
[14]
Familial adenomatous polyposis (FAP) patients Min mouse (C57BL/6J ApcMin/+-FCCC) Apc (germline mutation) backcrossed with C57BL/6JNIcr mouse Adenoma, adenocarcinoma (colon, small intestine)
[15,16]
Familial adenomatous polyposis (FAP) patients FAP rat model (Pirc rat [F344/N-Tac-Apcam1137]) ENU-induced point mutation results in truncating mutation in the Apc gene; corresponds to human mutation hotspot region Adenoma, adenocarcinoma (colon, small intestine)
[17-21]
Hereditary nonpolyposis colorectal cancer (Lynch syndrome) patients HNPCC/Lynch Syndrome mouse [C57BL/6J. Msh2fl/fl; Tg( Vil-Cre) or Msh2loxp/loxp. TgfβRIIhu/hu; Tg(Vil-Cre)] Villin-Cre-dependent Msh2 deletion in intestinal epithelium, with or without knock-in of a humanized TgfβRII coding exon 10 poly(A) repeat (to induce 1-3 colorectal adenomas and stage I CRC by 9 months of age) MMR-deficient adenoma/ adenocarcinoma
[22-24]
Hereditary colorectal cancer (support pending) CRC mouse model; CAC;Apc580S/+ mice Carbonic anhydrase I-driven Cre (CAC)- expression limited to the epithelial cells of the large intestine Adenoma, adenocarcinoma (large intestine)
[25]
Not applicable, targeting sporadic colorectal cancer (support pending) Colon-specific conditional KO mouse model (Apctm2Rak, Krastm4Tyj, Tp53tm2Tyj) Adenoviral-Cre induced inactivation of Apc, and activation of oncogenicgenes Kras(G12D) and Tp53(R172H) Adenoma, adenocarcinoma (distal colon)
[26]
Endometrium/ Uterus Endometrial hyperplasia patients Rat (Sprague-Dawley®) Ovariectomized/estrogen pellet implant Endometrial hyperplasia, atypical endometrial hyperplasia
[27,28]
Esophagus Barrett's esophagus patients Barrett's mouse (ED-L2-IL1β) Transgenic expression of modified human IL1β is driven by Epstein-Barr virus ED-L2 promoter. Barrett's-like metaplasia and progression to adenocarcinoma
[29,30]
Head and Neck Individuals at high risk for oral cancer Rat (F344) 4-NQO Squamous cell carcinoma
[31,32]
Liver Patients with NASH and cirrhosis under surveillance for HCC HepPten- mouse (C57BL/6-PtenloxP/loxP;Alb-Cre+) Hepatocyte-specific Pten deletion (HepPten-) induces hepatic steatosis, inflammation, fibrosis and tumors. Adenocarcinoma, hepatocellular carcinoma
[33]
Lung Individuals at high risk for lung cancer Mouse (A/J or A/J x UL53-3[F1]) B[a]P Adenoma, adenocarcinoma
[34-41]
Individuals at high risk for lung cancer Mouse (A/J or A/J x UL53-3[F1]) MNU Adenoma, adenocarcinoma
[42]
Individuals at high risk for lung cancer Mouse (A/J or A/J x UL53-3[F1]) Vinyl carbamate Adenoma, adenocarcinoma
[43]
Individuals at high risk for lung cancer Mouse (NIH Swiss) NTCU Squamous cell carcinoma
[38,39,44-51]
Current or former smokers at risk for lung cancer Mouse (A/J, Swiss H or Swiss ICR [CD-1]) Cigarette smoke (ECS or MCS) Adenoma, adenocarcinoma
[52-58]
Individuals at high risk for lung cancer A/J mouse (p53fl/f-Rb1fl/fl) Somatic inactivation of p53 and Rb1 in pulmonary bronchial epithelial cells by intratracheal Adeno-Cre Small cell lung cancer
[40,59]
Individuals at high risk for lung cancer A/J mouse (p53Ala135Val/+) Transgenic expression of mutant p53; lung tumor induction upon carcinogen administration Adenoma, adenocarcinoma
[60,61]
Subjects with a familial lung cancer susceptibility gene fingerprint B6 mouse (CCSP-EGFRL858R) Doxycycline-induced upregulation of oncogene EGFRL858R in type II pneumocytes only Adenocarcinoma
[62]
Subjects with a familial lung cancer susceptibility gene fingerprint CCSPCre mouse (129SvJ-C57BL/6.CCSPCre; KrasLSL-G12D) Cre recombinase under the control of the CCSP promoter activates KrasG12D mutant by removing the lox-stop-lox sequence in club cells (bronchiolar secretory cells) Adenocarcinoma, non-small cell lung cancer
[63]
Subjects with a familial lung cancer susceptibility gene fingerprint FVB mouse (CCSP-KrasG12D/+) KrasG12D mutated allele is expressed in type II pneumocytes after cross with Clara cell secreted protein strain and doxycycline induction Adenocarcinoma
[64-66]
Former smokers Mouse (NOD SCID) Xenograft, MDA-MB-231-Luc human mammary adenocarcinoma cells Proliferation biomarker  
Individuals at high risk for lung cancer Mouse (Nude, Athymic) Xenograft, H3255 human lung adenocarcinoma cells Proliferation biomarker
[39]
Mammary Gland Women at high risk for breast cancer Mouse (FVB.MMTV-ErbB2) DMBA Adenocarcinoma (ER- breast cancer model)
[67-71]
Women at high risk for breast cancer Rat (Sprague-Dawley®) DMBA Adenoma, adenocarcinoma (ER+ breast cancer model)
[69,72]
Women at high risk for breast cancer Rat (Sprague-Dawley®, young and 100 days old) MNU Adenocarcinoma (ER+ breast cancer model)
[70,73-81]
Subjects with BRCA-1 mutations or premalignant breast disease BRCA1 mouse (Brac1co/co or Brca1fl/fl-Trp53+/--MMTV-Cre) MMTV-Cre-dependent deletion of Brca1 on a Trp53+/- background (triple negative breast cancer model) Adenocarcinoma
[82,83]
Subjects with BRCA-2 mutations BRCA2 mouse (MMTV-Cre; Brca2fl/fl;p53fl/+) The Cre-loxP system obtained epithelium-specific deletion of Brca2 and the Tp53 tumor suppressor gene leads to mammary tumorigenesis Adenocarcinoma
[84]
Healthy individuals at risk for developing breast cancer FVB mouse (MMTV-PPARδ) Transgenic expression of PPARδ driven by mouse mammary tumor virus promoter/enhancer (ER+PR+HER2- breast cancer model) Adenocarcinoma
[85]
Women at high risk for breast cancer FVB mouse (MMTV-Neu) Transgenic expression of wild-type HER2/Neu under the transcriptional control of the mouse mammary tumor virus promoter/enhancer (ER-, HER2+ breast cancer model) Adenocarcinoma
[67,69,86]
Subjects with BRCA-1 mutations or at high risk of triple negative breast cancer FVB mouse (FVB-MMTV-Wnt1) Proto-oncogene Wnt-1 activated by mouse mammary tumor virus Preneoplastic lesion, tumor
[87]
Ductal carcinoma in situ patients FVB mouse (TgN[C3-1-TAg]cJeg) C3(1) 5' regulatory region of TAg targets expression to the mammary gland Preneoplastic lesion, tumor
[88,89]
Subjects with BRCA-1 mutations or at high risk of triple negative breast cancer BRCA1 mouse (BLG-Cre;Brca1F22-24/F22-24; p53+/-) Expression of the BLG-Cre transgene leads to loss of Brca1 function in the mammary gland and mutant p53 accelerates mammary tumor formation Adenocarcinoma, spindle, squamous carcinoma
[90]
Subjects with BRCA-1 mutations or at high risk of triple negative breast cancer Mouse (BALB/c) Syngeneic, p53-/- mammary tissue transplant Ductal adenocarcinoma (triple negative breast cancer)
[91]
Ductal carcinoma in situ patients Mouse (BALB/c) (MIND model) Intraductal injection of patient-derived DCIS cell lines DCIS lesions, invasive ductal carcinoma
[92]
Mesothelioma Asbestos-exposed individuals Mesothelioma mouse (FVB-Nf2+/--Cdkn2a+/-) Haploinsufficiency for Cdkn2a and Nf2 accelerates asbestos-induced malignant mesothelioma onset and progression Malignant mesothelioma in peritoneal, pleural, and pericardial tissues
[93]
Other, Solid Tumors P.I. cited "high-risk populations," but not specified Mouse (C57BL/6) Syngeneic, Lewis lung cancer cells and Syngeneic, MC38 mouse colon cancer cells Adenocarcinoma  
Ovary Not specified by PI but likely BRCA-1/2 carriers DKO mouse (Dicerfl/fl- Ptenfl/fl-Amhr2Cre) Amhr2-Cre-dependent deletion of Pten and Dicer High-grade serous carcinoma
[94,95]
Not specified by PI but likely BRCA-1/2 carriers DKO mouse (Dicerfl/fl- Ptenfl/fl) Inactivation of Dicer and Pten (double knockout) in the fallopian tube by intra-ovarian injection of Ad-mCherry-Cre High-grade serous carcinoma
[94-96]
Subjects with BRCA-1 mutations BRCA1 mouse (Brca1fl/fl- Tp53fl/fl-Ptenfl/fl-Pax8-Cre) Doxycycline-induced inactivation of Brca1, p53, and Pten in fallopian tube secretory epithelial cells by Pax8-Cre High-grade serous carcinoma
[97]
Subjects with BRCA-1 mutations Mouse (C57BL/6) Syngeneic, ID8-Luc cells Adenocarcinoma
[98]
Pancreas Individuals at high risk for pancreatic cancer iKras mouse (B6.FVB-Tg[p48Cre-R26-rtTa-IRES2-EGFP-TetO-KrasG12D]), and (C57BL/6-Tg[p48CRE-tetO-LSLKrasG12D-ROSA-rtTA-p53L/+]) p48-Cre allele drives Cre expression mostly in a pancreas-specific manner. The rtTa and EGFP are expressed in the pancreatic epithelium during embryogenesis and into adulthood. Activation of rtTa with doxycycline leads to mutant Kras expression. From the TetO-KrasG12D allele. PanINs, PDAC
[99]
Individuals at high risk for pancreatic cancer LSL-Kras (B6;129S4-LSL-KrasG12D/+ -p48Cre) p48-Cre-driven mutant KrasG12D expression PanIN to PDAC progression
[100-103]
Intraductal papillary mucinous neoplasm patients KCiHnf1b mouse (Hnf1b:CreERT2; LSL-KrasG12V) Oncogenic Kras is activated by tamoxifen in adult pancreatic ductal cells. IPMN, PanIN, PDAC
[104]
Intraductal papillary mucinous neoplasm patients KPSD4 mouse (C57BL/6J-Pdx1Cre+/--KrasG12D+/--Smad4-/-) Smad4 deficiency enables rapid progression of KrasG12D-initiated neoplasms progressing to pancreatic tumors IPMN progression to carcinoma
[100,105]
Individuals with PanIN lesions and or chronic pancreatitis KPC mouse (B6;129S4.LSL-KrasG12D/+-LSL-Trp53R172H/+-Ptf1acre-ERTM) Tamoxifen-induced activation of KrasG12D and p53 gene expression promote carcinogenesis PanIN to PDAC progression
[100,106]
Individuals with PanIN lesions and or chronic pancreatitis huMUC1 LSL-Kras mouse (B6;129S4.huMUC1+/--LSL-KrasG12D+-p48Cre) p48-Cre-driven mutant KrasG12D expression on a human MUC1 transgenic background PanIN to PDAC progression
[107]
Individuals with PanIN lesions and or chronic pancreatitis Mouse (C57BL/6) Syngeneic, KrasG12D;p53+/-;Cre (KCiHnf1b) pancreatic ductal adenocarcinoma cells Optimal dose determination prior to efficacy study with a GEMM
[104]
Prostate Individuals at high risk for prostate cancer Rat (Wistar or Wistar-Unilever) MNU Adenocarcinoma
[108,109]
Individuals at high risk for prostate cancer Hi-Myc mouse (FVB/ARR2/ probasin-Myc) Prostate-specific transgenic expression of Myc driven by ARR2/probasin promoter Pre-PIN, PIN, adenocarcinoma
[110]
Individuals at high risk for prostate cancer TMPRSS2-ERG driven mouse (FVB-Ptenflox/flox-R26ERG-Tg[CreERT2]) Tamoxifen-induced deletion of Pten specifically in the TMPRSS2-positive cells in the prostate Pre-PIN, PIN, adenocarcinoma
[111]
Urinary Bladder Subjects previously treated for non-muscle-invasive urinary bladder cancer Mouse (C57BL/6) OH-BBN Transitional cell carcinoma
[112,113]
Subjects previously treated for non-muscle-invasive urinary bladder cancer Rat (F344) OH-BBN Transitional cell carcinoma
[112-115]
Subjects previously treated for non-muscle-invasive urinary bladder cancer Mouse (C57BL/6) Syngeneic, MB49 urothelial carcinoma cells Tumor growth, immunogenicity to vaccine  

Carcinogen abbreviations

4-NQO = 4-nitroquinoline-1-oxide
AOM = azoxymethane
B[a]P = benzo[a]pyrene
DMBA = dimethylbenz[a]anthracene
DSS = dextran sulfate sodium
ECS = environmental cigarette smoke
ENU = N-ethyl-N-nitrosourea
MCS = mainstream cigarette smoke
MNU = methylnitrosourea
NTCU = N-nitrosotris(2-chloroethyl) urea
OH-BBN = N-butyl-N-(4-hydroxylbutyl)nitrosamine
TNBS = 2,4,6-trinitrobenzene sulfonic acid

Phenotypic/genetic abbreviations

ACF = aberrant crypt foci
APC = adenomatous polyposis coli
ARR = androgen response elements
CCSP = club cell secretory protein
DCIS = ductal carcinoma in situ
EGFP = enhanced green fluorescent protein
HER2 = human epidermal growth factor receptor 2
HNPCC = hereditary nonpolyposis colorectal cancer
IPMN = intraductal papillary mucinous neoplasm
MIND = mammary intraductal
MMR = mismatch repair
MMTV = mouse mammary tumor virus
Msh2 = mutS homolog 2
MUC1 = mucin1
PanIN = pancreatic intraepithelial neoplasia
PDAC = pancreatic ductal adenocarcinoma
PIN = prostatic intraepithelial neoplasia
PPAR = peroxisome proliferator-activated receptor
rtTa = reverse tetracycline transactivator
TAg = large tumor antigen
TMPRSS2 = transmembrane serine protease 2

References

Literature information on models and PREVENT publications where specified model(s) were used.

  1. Rosenberg DW, Giardina C, Tanaka T. Mouse models for the study of colon carcinogenesis. Carcinogenesis 2009;30:183–96.
  2. Rao CV, Madka V, Zhang Y, Pathuri G, Panneerselvam J, Stratton N, Finnberg NK, Safran HP, Fox J, Sei S, Glaze ER, Shoemaker R, El-Deiry WS. Abstract 14: TRAIL inducing small molecule ONC201 prevents intestinal tumors in FAP mouse model. Cancer Res 2020;80 (16 Suppl):abstr 14.
  3. Reddy BS, Wang CX, Kong AN, Khor TO, Zheng X, Steele VE, Kopelovich L, Rao CV. Prevention of azoxymethane-induced colon cancer by combination of low doses of atorvastatin, aspirin, and celecoxib in F 344 rats. Cancer Res 2006;66:4542–6.
  4. Wargovich MJ, Chen CD, Jimenez A, Steele VE, Velasco M, Stephens LC, Price R, Gray K, Kelloff GJ. Aberrant crypts as a biomarker for colon cancer: evaluation of potential chemopreventive agents in the rat. Cancer Epidemiol Biomarkers Prev 1996;5:355–60.
  5. Mohammed A, Janakiram NB, Madka V, Zhang Y, Singh A, Biddick L, Li Q, Lightfoot S, Steele VE, Lubet RA, Suen CS, Miller MS, Sei S, Rao CV. Intermittent Dosing Regimens of Aspirin and Naproxen Inhibit Azoxymethane-Induced Colon Adenoma Progression to Adenocarcinoma and Invasive Carcinoma. Cancer Prev Res (Phila) 2019;12:751–62.
  6. Madka V, Zhang Y, Pathuri G, Panneerselvam J, Stratton N, Singh A, Sei S, Fox J, Rao CV. Abstract 15: Hypertension drug Olmesartan medoxomil promotes colonic tumorigenesis in AOM-induced CRC rat model. Cancer Res 2020;80 (16 Suppl):abstr 15.
  7. Janakiram NB, Mohammed A, Pathuri G, Madka V, Ritchie R, Bryant T, Zhang Y, Li Q, Lightfoot S, Gali H, Vernon SE, Suen CS, Rao CV. Abstract 2604: Chemoprevention of colorectal cancer by LFA-9, a novel dual mPGES-1/5-LOX inhibitor: safer approaches to chemoprevention. Cancer Res 2016;76 (14 Suppl):abstr 2604.
  8. Mohammed A, Patlolla JMR, Zhang Y, Biddick L, Madka V, Li Q, Lightfoot S, Lubet R, Suen CS, Steele VE, Rao CV. Abstract 2820: Omeprazole alone, or in combination with Aspirin inhibits azoxymethane-induced colon adenoma progression to adenocarcinoma and carcinoma invasion in F344 rat model. Cancer Res 2015;75 (15 Suppl):abstr 2820.
  9. Mohammed A, Janakiram NB, Madka V, Zhang Y, Singh A, Biddick L, Li Q, Lightfoot S, Steele VE, Lubet R, Miller MS, Suen CS, Sei S, Rao CV. Abstract 4983: Intermittent dosing regimens of naproxen and aspirin inhibit azoxymethane-induced rat colon adenoma progression to adenocarcinoma and carcinoma invasion. Cancer Res 2018;78 (13 Suppl):abstr 4983.
  10. Osawa E, Nakajima A, Fujisawa T, Kawamura YI, Toyama-Sorimachi N, Nakagama H, Dohi T. Predominant T helper type 2-inflammatory responses promote murine colon cancers. Int J Cancer 2006;118:2232–6.
  11. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, Luongo C, Gould KA, Dove WF. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 1992;256:668–70.
  12. Montrose DC, Zhou XK, McNally EM, Sue E, Yantiss RK, Gross SS, Leve ND, Karoly ED, Suen CS, Ling L, Benezra R, Pamer EG, Dannenberg AJ. Celecoxib alters the intestinal microbiota and metabolome in association with reducing polyp burden. Cancer Prev Res (Phila) 2016;9:721–31.
  13. Disis ML, Corulli LR, Grubbs C, Lubet RA, Cowan P, Gad E. Abstract 1266: Downregulation of PD-L1 by NSAID administration augments the effects of a multi-antigen vaccine for the prevention of adenomatous polyps in APC(Min/+) mice. Cancer Res 2018;78 (13 Suppl):abstr 1266.
  14. Moser AR, Dove WF, Roth KA, Gordon JI. The Min (multiple intestinal neoplasia) mutation: its effect on gut epithelial cell differentiation and interaction with a modifier system. J Cell Biol 1992;116:1517–26.
  15. Cooper HS, Chang WC, Coudry R, Gary MA, Everley L, Spittle CS, Wang H, Litwin S, Clapper ML. Generation of a unique strain of multiple intestinal neoplasia (Apc(+/Min-FCCC)) mice with significantly increased numbers of colorectal adenomas. Mol Carcinog 2005;44:31–41.
  16. Chang W-CL, Kaunga E, Cooper HS, Vanderveer L, Peng J, Zhang Y, Suen CS, Clapper ML. Abstract 2806: Effect of ED-71, an analogue of Vitamin D3, on intestinal neoplasia in the Apc+/Min-FCCC mouse model. Cancer Res 2015;75 (15 Suppl):abstr 2806.
  17. Amos-Landgraf JM, Irving AA, Hartman C, Hunter A, Laube B, Chen X, Clipson L, Newton MA, Dove WF. Monoallelic silencing and haploinsufficiency in early murine intestinal neoplasms. Proc Natl Acad Sci U S A 2012;109:2060–5.
  18. Amos-Landgraf JM, Kwong LN, Kendziorski CM, Reichelderfer M, Torrealba J, Weichert J, Haag JD, Chen KS, Waller JL, Gould MN, Dove WF. A target-selected Apc-mutant rat kindred enhances the modeling of familial human colon cancer. Proc Natl Acad Sci U S A 2007;104:4036–41.
  19. Ulusan AM, Rajendran P, Dashwood WM, Yavuz OF, Kapoor S, Gustafson TA, Savage MI, Brown PH, Sei S, Mohammed A, Vilar E, Dashwood RH. Optimization of erlotinib plus sulindac dosing regimens for intestinal cancer prevention in an Apc-mutant model of familial adenomatous polyposis (FAP). Cancer Prev Res (Phila) 2021;14:325–36.
  20. Rajendran P, Ulusan A, Dashwood W-M, Kapoor S, Mohammed A, Sei S, Rashid A, Brown PH, Vilar-Sanchez E, Dashwood RH. Abstract 21: Optimization of dosing regimens of sulindac in combination with erlotinib for small intestine and colorectal cancer prevention. Cancer Res 2020;80 (16 Suppl):abstr 21.
  21. Ulusan A, Rajendran P, Dashwood W-M, Mohammed A, Sei S, Brown PH, Vilar-Sanchez E, Dashwood RH. Abstract 5074: Optimizing erlotinib plus sulindac dosing regimens in a preclinical model of FAP. Cancer Res 2019;79 (13 Suppl):abstr 5074.
  22. Kucherlapati MH, Lee K, Nguyen AA, Clark AB, Hou H, Jr., Rosulek A, Li H, Yang K, Fan K, Lipkin M, Bronson RT, Jelicks L, Kunkel TA, Kucherlapati R, Edelmann W. An Msh2 conditional knockout mouse for studying intestinal cancer and testing anticancer agents. Gastroenterology 2010;138:993–1002.e1.
  23. Reyes-Uribe L, Wu W, Gelincik O, Bommi PV, Francisco-Cruz A, Solis LM, Lynch PM, Lim R, Stoffel EM, Kanth P, Samadder NJ, Mork ME, Taggart MW, Milne GL, Marnett LJ, Vornik L, Liu DD, Revuelta M, Chang K, You YN, Kopelovich L, Wistuba II, Lee JJ, Sei S, Shoemaker RH, Szabo E, Richmond E, Umar A, Perloff M, Brown PH, Lipkin SM, Vilar E. Naproxen chemoprevention promotes immune activation in Lynch syndrome colorectal mucosa. Gut 2021;70:555–82.
  24. Kloor M, Oezcan M, Ahadova A, Yuan Y, Bork P, Sei S, Shoemaker R, Gelincik O, Lipkin S, Gebert J, Doeberitz MvK. Abstract 717: Mouse model for the development of preventive and therapeutic vaccines against microsatellite-unstable cancers. Cancer Res 2018;78 (13 Suppl):abstr 717.
  25. Xue Y, Johnson R, Desmet M, Snyder PW, Fleet JC. Generation of a transgenic mouse for colorectal cancer research with intestinal cre expression limited to the large intestine. Mol Cancer Res 2010;8:1095–104.
  26. Betzler AM, Kochall S, Blickensdörfer L, Garcia SA, Thepkaysone ML, Nanduri LK, Muders MH, Weitz J, Reissfelder C, Schölch S. A genetically engineered mouse model of sporadic colorectal cancer. J Vis Exp 2017;(125):55952.
  27. Chandra V, Rai R, Hussain S, Garcia L, Hatipoglu M, Benbrook D. Abstract 27: Development of a rat model of atypical endometrial hyperplasia and a vaginal suppository formulation of SHetA2 for chemoprevention studies. Cancer Res 2020;80 (16 Suppl):abstr 27.
  28. Chandra V, Rai R, Lightfoot SS, Hatipoglu MK, Garcia-Contreras L, Benbrook DM. Abstract PO040: Chemoprevention and regression of estrogen-induced atypical endometrial hyperplasia by oral SHetA2 in a rat model. Clin Cancer Res 2021;27 (3 Suppl):abstr PO040.
  29. Quante M, Bhagat G, Abrams JA, Marache F, Good P, Lee MD, Lee Y, Friedman R, Asfaha S, Dubeykovskaya Z, Mahmood U, Figueiredo JL, Kitajewski J, Shawber C, Lightdale CJ, Rustgi AK, Wang TC. Bile acid and inflammation activate gastric cardia stem cells in a mouse model of Barrett-like metaplasia. Cancer Cell 2012;21:36–51.
  30. Münch NS, Fang HY, Ingermann J, Maurer HC, Anand A, Kellner V, Sahm V, Wiethaler M, Baumeister T, Wein F, Einwächter H, Bolze F, Klingenspor M, Haller D, Kavanagh M, Lysaght J, Friedman R, Dannenberg AJ, Pollak M, Holt PR, Muthupalani S, Fox JG, Whary MT, Lee Y, Ren TY, Elliot R, Fitzgerald R, Steiger K, Schmid RM, Wang TC, Quante M. High-fat diet accelerates carcinogenesis in a mouse model of barrett's esophagus via interleukin 8 and alterations to the gut microbiome. Gastroenterology 2019;157:492–506.e2.
  31. McCormick DL, Phillips JM, Horn TL, Johnson WD, Steele VE, Lubet RA. Overexpression of cyclooxygenase-2 in rat oral cancers and prevention of oral carcinogenesis in rats by selective and nonselective COX inhibitors. Cancer Prev Res (Phila) 2010;3:73–81.
  32. McCormick DL, Horn TL, Johnson WD, Peng X, Lubet RA, Steele VE. Suppression of rat oral carcinogenesis by agonists of peroxisome proliferator activated receptor . PLoS One 2015;10:e0141849.
  33. Horie Y, Suzuki A, Kataoka E, Sasaki T, Hamada K, Sasaki J, Mizuno K, Hasegawa G, Kishimoto H, Iizuka M, Naito M, Enomoto K, Watanabe S, Mak TW, Nakano T. Hepatocyte-specific Pten deficiency results in steatohepatitis and hepatocellular carcinomas. J Clin Invest 2004;113:1774–83.
  34. Gunning WT, Kramer PM, Lubet RA, Steele VE, End DW, Wouters W, Pereira MA. Chemoprevention of benzo(a)pyrene-induced lung tumors in mice by the farnesyltransferase inhibitor R115777. Clin Cancer Res 2003;9:1927–30.
  35. Galbraith AR, Seabloom DE, Wuertz BR, Antonides JD, Steele VE, Wattenberg LW, Ondrey FG. Chemoprevention of lung carcinogenesis by dietary nicotinamide and inhaled budesonide. Cancer Prev Res (Phila) 2019;12:69–78.
  36. Seabloom DE, Galbraith AR, Haynes AM, Antonides JD, Wuertz BR, Miller WA, Miller KA, Steele VE, Miller MS, Clapper ML, O'Sullivan MG, Ondrey FG. Fixed-dose combinations of pioglitazone and metformin for lung cancer prevention. Cancer Prev Res (Phila) 2017;10:116–23.
  37. Seabloom DE, Galbraith AR, Haynes AM, Antonides JD, Wuertz BR, Miller WA, Miller KA, Steele VE, Suen CS, O'Sullivan MG, Ondrey FG. Safety and preclinical efficacy of aerosol pioglitazone on lung adenoma prevention in A/J mice. Cancer Prev Res (Phila) 2017;10:124–32.
  38. Zhang Q, Lee SB, Chen X, Stevenson ME, Pan J, Xiong D, Zhou Y, Miller MS, Lubet RA, Wang Y, Mirza SP, You M. Optimized bexarotene aerosol formulation inhibits major subtypes of lung cancer in mice. Nano Lett 2019;19:2231–42.
  39. Zhang Q, Li R, Chen X, Lee SB, Pan J, Xiong D, Hu J, Miller MS, Szabo E, Lubet RA, Wang Y, You M. Effect of weekly or daily dosing regimen of Gefitinib in mouse models of lung cancer. Oncotarget 2017;8:72447–56.
  40. Zhang Q, Pan J, Miller MS, Lubet RA, Wang Y, You M. Abstract 188: Preventive effect of aerosolized bexarotene in three major subtypes of lung cancer: adenocarcinoma, squamous cell carcinoma and small cell lung cancer in mice. Cancer Res 2017;77 (13 Suppl):abstr 188.
  41. Xiong D, Pan J, Zhang Q, Szabo E, Miller MS, Lubet RA, Wang Y, You M. Pioglitazone-mediated reversal of elevated glucose metabolism in the airway epithelium of mouse lung adenocarcinomas. JCI Insight 2017;2:e94220.
  42. Gunning WT, Castonguay A, Goldblatt PJ, Stoner GD. Strain A/J mouse lung adenoma growth patterns vary when induced by different carcinogens. Toxicol Pathol 1991;19:168–75.
  43. Foley JF, Anderson MW, Stoner GD, Gaul BW, Hardisty JF, Maronpot RR. Proliferative lesions of the mouse lung: progression studies in strain A mice. Exp Lung Res 1991;17:157–68.
  44. Lijinsky W, Winter C. Skin tumors induced by painting nitrosoalkylureas on mouse skin. J Cancer Res Clin Oncol 1981;102:13–20.
  45. Pan J, Zhang Q, Li K, Liu Q, Wang Y, You M. Chemoprevention of lung squamous cell carcinoma by ginseng. Cancer Prev Res (Phila) 2013;6:530–9.
  46. Wang Y, Zhang Z, Yan Y, Lemon WJ, LaRegina M, Morrison C, Lubet R, You M. A chemically induced model for squamous cell carcinoma of the lung in mice: histopathology and strain susceptibility. Cancer Res 2004;64:1647–54.
  47. Zhou Y, Zhang Q, Du M, Xiong D, Wang Y, Mohammed A, Lubet RA, Wang L, You M. Exosomal miRNAs as novel pharmacodynamic biomarkers for cancer chemopreventive agent early stage treatments in chemically induced mouse model of lung squamous cell carcinoma. Cancers (Basel) 2019;11:477.
  48. Riolobos L, Gad EA, Treuting PM, Timms AE, Hershberg EA, Corulli LR, Rodmaker E, Disis ML. The effect of mouse strain, sex, and carcinogen dose on toxicity and the development of lung dysplasia and squamous cell carcinomas in mice. Cancer Prev Res (Phila) 2019;12:507–16.
  49. Xiong D, Pan J, Yin Y, Jiang H, Szabo E, Lubet RA, Wang Y, You M. Novel mutational landscapes and expression signatures of lung squamous cell carcinoma. Oncotarget 2018;9:7424–41.
  50. Pan J, Xiong D, Zhang Q, Szabo E, Miller MS, Lubet RA, Wang Y, You M. Airway brushing as a new experimental methodology to detect airway gene expression signatures in mouse lung squamous cell carcinoma. Sci Rep 2018;8:8895.
  51. Xiong D, Pan J, Zhang Q, Szabo E, Miller MS, Lubet RA, You M, Wang Y. Bronchial airway gene expression signatures in mouse lung squamous cell carcinoma and their modulation by cancer chemopreventive agents. Oncotarget 2017;8:18885–900.
  52. Hecht SS. Tobacco smoke carcinogens and lung cancer. J Natl Cancer Inst 1999;91:1194–210.
  53. De Flora S, Ganchev G, Iltcheva M, La Maestra S, Micale RT, Steele VE, Balansky R. Pharmacological modulation of lung carcinogenesis in smokers: Preclinical and clinical evidence. Trends Pharmacol Sci 2016;37:120–42.
  54. Balansky R, Ganchev G, Iltcheva M, Micale RT, La Maestra S, D'Oria C, Steele VE, De Flora S. Selective inhibition by aspirin and naproxen of mainstream cigarette smoke-induced genotoxicity and lung tumors in female mice. Arch Toxicol 2016;90:1251–60.
  55. La Maestra S, D'Agostini F, Izzotti A, Micale RT, Mastracci L, Camoirano A, Balansky R, Trosko JE, Steele VE, De Flora S. Modulation by aspirin and naproxen of nucleotide alterations and tumors in the lung of mice exposed to environmental cigarette smoke since birth. Carcinogenesis 2015;36:1531–8.
  56. Izzotti A, Longobardi M, La Maestra S, Micale RT, Pulliero A, Camoirano A, Geretto M, D'Agostini F, Balansky R, Miller MS, Steele VE, De Flora S. Release of microRNAs into body fluids from ten organs of mice exposed to cigarette smoke. Theranostics 2018;8:2147–60.
  57. Izzotti A, Balansky R, Ganchev G, Iltcheva M, Longobardi M, Pulliero A, Geretto M, Micale RT, La Maestra S, Miller MS, Steele VE, De Flora S. Blood and lung microRNAs as biomarkers of pulmonary tumorigenesis in cigarette smoke-exposed mice. Oncotarget 2016;7:84758–74.
  58. Izzotti A, Balansky R, Ganchev G, Iltcheva M, Longobardi M, Pulliero A, Camoirano A, D'Agostini F, Geretto M, Micale RT, La Maestra S, Miller MS, Steele VE, De Flora S. Early and late effects of aspirin and naproxen on microRNAs in the lung and blood of mice, either unexposed or exposed to cigarette smoke. Oncotarget 2017;8:85716–48.
  59. Wang Y, Wen W, Yi Y, Zhang Z, Lubet RA, You M. Preventive effects of bexarotene and budesonide in a genetically engineered mouse model of small cell lung cancer. Cancer Prev Res (Phila) 2009;2:1059–64.
  60. Wang Y, Rouggly L, You M, Lubet R. Animal models of lung cancer characterization and use for chemoprevention research. Prog Mol Biol Transl Sci 2012;105:211–26.
  61. Zhang Z, Liu Q, Lantry LE, Wang Y, Kelloff GJ, Anderson MW, Wiseman RW, Lubet RA, You M. A germ-line p53 mutation accelerates pulmonary tumorigenesis: p53-independent efficacy of chemopreventive agents green tea or dexamethasone/myo-inositol and chemotherapeutic agents taxol or adriamycin. Cancer Res 2000;60:901–7.
  62. Politi K, Zakowski MF, Fan PD, Schonfeld EA, Pao W, Varmus HE. Lung adenocarcinomas induced in mice by mutant EGF receptors found in human lung cancers respond to a tyrosine kinase inhibitor or to down-regulation of the receptors. Genes Dev 2006;20:1496–510.
  63. Moghaddam SJ, Li H, Cho SN, Dishop MK, Wistuba, II, Ji L, Kurie JM, Dickey BF, Demayo FJ. Promotion of lung carcinogenesis by chronic obstructive pulmonary disease-like airway inflammation in a K-ras-induced mouse model. Am J Respir Cell Mol Biol 2009;40:443–53.
  64. Fisher GH, Wellen SL, Klimstra D, Lenczowski JM, Tichelaar JW, Lizak MJ, Whitsett JA, Koretsky A, Varmus HE. Induction and apoptotic regression of lung adenocarcinomas by regulation of a K-Ras transgene in the presence and absence of tumor suppressor genes. Genes Dev 2001;15:3249–62.
  65. Pan J, Zhang Q, Sei S, Shoemaker RH, Lubet RA, Wang Y, You M. Immunoprevention of KRAS-driven lung adenocarcinoma by a multipeptide vaccine. Oncotarget 2017;8:82689–99.
  66. Pan J, Zhang Q, Sei S, Shoemaker RH, Lubet RA, Wang Y, You M. Abstract 1698: Immunoprevention of KRAS-driven lung adenocarcinoma by a multi-peptide KRAS vaccine. Cancer Res 2017;77 (13 Suppl):abstr 1698.
  67. Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, Muller WJ. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc Natl Acad Sci U S A 1992;89:10578–82.
  68. Yin Y, Bai R, Russell RG, Beildeck ME, Xie Z, Kopelovich L, Glazer RI. Characterization of medroxyprogesterone and DMBA-induced multilineage mammary tumors by gene expression profiling. Mol Carcinog 2005;44:42–50.
  69. Shoemaker RH, Fox JT, Juliana MM, Moeinpour FL, Grubbs CJ. Evaluation of the STAT3 inhibitor GLG302 for the prevention of estrogen receptorpositive and negative mammary cancers. Oncol Rep 2019;42:1205–13.
  70. Mohammed A, Sei S, Shoemaker R, Grubbs CJ. Abstract 1099: Combination of bazedoxifene and lapatinib profoundly inhibits estrogen receptor positive (ER+) and negative (ER-) mammary tumorigenesis. Cancer Res 2020;80 (16 Suppl):abstr 1099.
  71. Dunn BK, Suen C, Grubbs C. Abstract 1250: Evaluation of the prevention by pioglitazone/metformin of ER-positive and ER-negative mammary cancers occurring in rodents on a high-fat diet. Cancer Res 2018;78 (13 Suppl):abstr 1250.
  72. Grubbs CJ, Steele VE, Casebolt T, Juliana MM, Eto I, Whitaker LM, Dragnev KH, Kelloff GJ, Lubet RL. Chemoprevention of chemically-induced mammary carcinogenesis by indole-3-carbinol. Anticancer Res 1995;15:709–16.
  73. Cha RS, Thilly WG, Zarbl H. N-nitroso-N-methylurea-induced rat mammary tumors arise from cells with preexisting oncogenic Hras1 gene mutations. Proc Natl Acad Sci U S A 1994;91:3749–53.
  74. McCormick DL, Adamowski CB, Fiks A, Moon RC. Lifetime dose-response relationships for mammary tumor induction by a single administration of N-methyl-N-nitrosourea. Cancer Res 1981;41:1690–4.
  75. Dunn BK, Suen C, Lubet RA, Steele VE, Grubbs CJ. Abstract 5246: Effects of bazedoxifene either alone or in combination with letrozole in the prevention of chemically induced mammary cancers. Cancer Res 2017;77 (13 Suppl):abstr 5246.
  76. Miller MS, Grubbs CJ, Stirdivant S, Lubet RA. Abstract 5255: Comparison of high-fructose and standard diets in methylnitrosourea (MNU)-induced ER+ mammary cancers: Altered carcinogenesis, differential effects of metformin, and metabolomic differences. Cancer Res 2017;77 (13 Suppl):abstr 5255.
  77. Dunn BK, Grubbs CJ. Abstract P5-14-02: Effects of bazedoxifene and/or letrozole in the prevention of chemically-induced mammary cancers. Cancer Res 2018;78 (4 Suppl):abstr P5–14–02.
  78. Lubet RA, Beger RD, Miller MS, Luster J, Seifried HE, Grubbs CJ. Comparison of effects of diet on mammary cancer: Efficacy of various preventive agents and metabolomic changes of different diets and agents. Cancer Prev Res (Phila) 2018;11:831–40.
  79. Kumar A, Lubet RA, Fox JT, Nelson WG, Seifried H, Grubbs CJ, Miller MS. Effects of high-fructose diet vs. Teklad diet in the MNU-induced rat mammary cancer model: Altered tumorigenesis, metabolomics and tumor RNA expression. J Obes Chronic Dis 2021;5:67–78.
  80. Cao Z, Miller MS, Lubet RA, Grubbs CJ, Beger RD. Pharmacometabolomic pathway response of effective anticancer agents on different diets in rats with induced mammary tumors. Metabolites 2019;9:149.
  81. Lubet RA, Heckman-Stoddard BM, Fox JT, Moeinpour F, Juliana MM, Shoemaker RH, Grubbs CJ. Use of biomarker modulation in normal mammary epithelium as a correlate for efficacy of chemopreventive agents against chemically induced cancers. Cancer Prev Res (Phila) 2020;13:283–90.
  82. Liu X, Holstege H, van der Gulden H, Treur-Mulder M, Zevenhoven J, Velds A, Kerkhoven RM, van Vliet MH, Wessels LF, Peterse JL, Berns A, Jonkers J. Somatic loss of BRCA1 and p53 in mice induces mammary tumors with features of human BRCA1-mutated basal-like breast cancer. Proc Natl Acad Sci U S A 2007;104:12111–6.
  83. Xu X, Qiao W, Linke SP, Cao L, Li WM, Furth PA, Harris CC, Deng CX. Genetic interactions between tumor suppressors Brca1 and p53 in apoptosis, cell cycle and tumorigenesis. Nat Genet 2001;28:266–71.
  84. Jonkers J, Meuwissen R, van der Gulden H, Peterse H, van der Valk M, Berns A. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat Genet 2001;29:418–25.
  85. Yuan H, Lu J, Xiao J, Upadhyay G, Umans R, Kallakury B, Yin Y, Fant ME, Kopelovich L, Glazer RI. PPARdelta induces estrogen receptor-positive mammary neoplasia through an inflammatory and metabolic phenotype linked to mTOR activation. Cancer Res 2013;73:4349–61.
  86. Shoemaker RH, Lovell MW, Whalen JJ, Moeinpour F, Grubbs CJ. Abstract 4657: Targeting STAT3 for mammary cancer prevention in MMTV/Neu mice employing the antagonist GLG-302. Cancer Res 2015;75 (15 Suppl):abstr 4657.
  87. Li Y, Hively WP, Varmus HE. Use of MMTV-Wnt-1 transgenic mice for studying the genetic basis of breast cancer. Oncogene 2000;19:1002–9.
  88. Maroulakou IG, Anver M, Garrett L, Green JE. Prostate and mammary adenocarcinoma in transgenic mice carrying a rat C3(1) simian virus 40 large tumor antigen fusion gene. Proc Natl Acad Sci U S A 1994;91:11236–40.
  89. Wang Y. Abstract 4563: Immunoprevention of triple negative breast cancer by a multi-antigen, multi-peptide vaccine. Cancer Res 2020;80 (16 Suppl):abstr 4563.
  90. McCarthy A, Savage K, Gabriel A, Naceur C, Reis-Filho JS, Ashworth A. A mouse model of basal-like breast carcinoma with metaplastic elements. J Pathol 2007;211:389–98.
  91. Jerry DJ, Kittrell FS, Kuperwasser C, Laucirica R, Dickinson ES, Bonilla PJ, Butel JS, Medina D. A mammary-specific model demonstrates the role of the p53 tumor suppressor gene in tumor development. Oncogene 2000;19:1052–58.
  92. Behbod F, Kittrell FS, LaMarca H, Edwards D, Kerbawy S, Heestand JC, Young E, Mukhopadhyay P, Yeh HW, Allred DC, Hu M, Polyak K, Rosen JM, Medina D. An intraductal human-in-mouse transplantation model mimics the subtypes of ductal carcinoma in situ. Breast Cancer Res 2009;11:R66.
  93. Altomare DA, Vaslet CA, Skele KL, De Rienzo A, Devarajan K, Jhanwar SC, McClatchey AI, Kane AB, Testa JR. A mouse model recapitulating molecular features of human mesothelioma. Cancer Res 2005;65:8090–5.
  94. Kim J, Coffey DM, Creighton CJ, Yu Z, Hawkins SM, Matzuk MM. High-grade serous ovarian cancer arises from fallopian tube in a mouse model. Proc Natl Acad Sci U S A 2012;109:3921–6.
  95. Sharma K, Yin C, Kamat K, Repellin C, Sambucetti LC, Scholler N. Abstract LB-135: New cancer prevention model using imaging for early detection of mesothelin-expressing cancers. Cancer Res 2017;77 (13 Suppl):abstr LB–135.
  96. Kim J, Coffey DM, Ma L, Matzuk MM. The ovary is an alternative site of origin for high-grade serous ovarian cancer in mice. Endocrinology 2015;156:1975–81.
  97. Perets R, Wyant GA, Muto KW, Bijron JG, Poole BB, Chin KT, Chen JY, Ohman AW, Stepule CD, Kwak S, Karst AM, Hirsch MS, Setlur SR, Crum CP, Dinulescu DM, Drapkin R. Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in Brca;Tp53;Pten models. Cancer Cell 2013;24:751–65.
  98. Scholler N, Stein P, Repellin C, Kamat K, Harrison MT, Shoemaker R, Sambucetti L. Mesothelin Vaccination for the Prevention of Ovarian Cancer. J Immunol 2016;196 (1 Suppl):abstr 214.8.
  99. Collins MA, Bednar F, Zhang Y, Brisset JC, Galban S, Galban CJ, Rakshit S, Flannagan KS, Adsay NV, Pasca di Magliano M. Oncogenic Kras is required for both the initiation and maintenance of pancreatic cancer in mice. J Clin Invest 2012;122:639–53.
  100. Herreros-Villanueva M, Hijona E, Cosme A, Bujanda L. Mouse models of pancreatic cancer. World J Gastroenterol 2012;18:1286–94.
  101. Mohammed A, Janakiram NB, Li Q, Madka V, Ely M, Lightfoot S, Crawford H, Steele VE, Rao CV. The epidermal growth factor receptor inhibitor gefitinib prevents the progression of pancreatic lesions to carcinoma in a conditional LSL-KrasG12D/+ transgenic mouse model. Cancer Prev Res (Phila) 2010;3:1417–26.
  102. Mohammed A, Janakiram NB, Suen C, Stratton N, Lightfoot S, Singh A, Pathuri G, Ritchie R, Madka V, Rao CV. Targeting cholecystokinin-2 receptor for pancreatic cancer chemoprevention. Mol Carcinog 2019;58:1908–18.
  103. Mohammed A, Janakiram NB, Madka V, Pathuri G, Li Q, Ritchie R, Biddick L, Kutche H, Zhang Y, Singh A, Gali H, Lightfoot S, Steele VE, Suen CS, Rao CV. Lack of chemopreventive effects of P2X7R inhibitors against pancreatic cancer. Oncotarget 2017;8:97822–34.
  104. Bailey JM, Hendley AM, Lafaro KJ, Pruski MA, Jones NC, Alsina J, Younes M, Maitra A, McAllister F, Iacobuzio-Donahue CA, Leach SD. p53 mutations cooperate with oncogenic Kras to promote adenocarcinoma from pancreatic ductal cells. Oncogene 2016;35:4282–8.
  105. Kumar G, Madka V, Singh A, Kumar N, Stratton N, Lightfoot S, Mohammed A, Miller MS, Rao CV. Abstract 1102: Model optimization and chemoprevention of IPMN driven PDAC in KPSD4 mouse model. Cancer Res 2020;80 (16 Suppl):abstr 1102.
  106. Mohammed A, Madka V, Kumar G, Singh A, Stratton N, Lightfoot S, Miller MS, Rao CV. Abstract 13: Aspirin and metformin combination inhibits PDAC progression and metastasis in KPC mice. Cancer Res 2020;80 (16 Suppl):abstr 13.
  107. Tinder TL, Subramani DB, Basu GD, Bradley JM, Schettini J, Million A, Skaar T, Mukherjee P. MUC1 enhances tumor progression and contributes toward immunosuppression in a mouse model of spontaneous pancreatic adenocarcinoma. J Immunol 2008;181:3116–25.
  108. Bosland MC. Animal models for the study of prostate carcinogenesis. J Cell Biochem Suppl 1992;16h:89–98.
  109. McCormick DL, Johnson WD, Haryu TM, Bosland MC, Lubet RA, Steele VE. Null effect of dietary restriction on prostate carcinogenesis in the Wistar-Unilever rat. Nutr Cancer 2007;57:194–200.
  110. Ellwood-Yen K, Graeber TG, Wongvipat J, Iruela-Arispe ML, Zhang J, Matusik R, Thomas GV, Sawyers CL. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell 2003;4:223–38.
  111. Chen Y, Chi P, Rockowitz S, Iaquinta PJ, Shamu T, Shukla S, Gao D, Sirota I, Carver BS, Wongvipat J, Scher HI, Zheng D, Sawyers CL. ETS factors reprogram the androgen receptor cistrome and prime prostate tumorigenesis in response to PTEN loss. Nat Med 2013;19:1023–9.
  112. Lubet RA, Scheiman JM, Bode A, White J, Minasian L, Juliana MM, Boring DL, Steele VE, Grubbs CJ. Prevention of chemically induced urinary bladder cancers by naproxen: protocols to reduce gastric toxicity in humans do not alter preventive efficacy. Cancer Prev Res (Phila) 2015;8:296–302.
  113. Vasconcelos-Nobrega C, Colaco A, Lopes C, Oliveira PA. Review: BBN as an urothelial carcinogen. In Vivo 2012;26:727–39.
  114. Mohammed A, Miller MS, Lubet RA, Suen CS, Sei S, Shoemaker RH, Juliana MM, Moeinpour FL, Grubbs CJ. Combination of erlotinib and naproxen employing pulsatile or intermittent dosing profoundly inhibits urinary bladder cancers. Cancer Prev Res (Phila) 2020;13:273–82.
  115. Mohammed A, Miller MS, Lubet RA, Suen C, Sei S, Shoemaker RH, Grubbs CJ. Abstract 4989: Efficacy of erlotinib and/or naproxen when administered by intermittent dosing schedules in the prevention of chemically induced urinary bladder cancers. Cancer Res 2018;78 (13 Suppl):abstr 4989.