Aloysius J. Klingelhutz, PhD

Portrait
Professor of Microbiology and Immunology
Professor of Radiation Oncology

Contact Information

Office: 3-612 Bowen Science Building
51 Newton Rd
Iowa City, IA 52242
319-335-7788

Lab: 3-615A Bowen Science Building
51 Newton Rd
Iowa City, IA 52242
319-335-8499

Education

BS, Biology, St John's University
PhD, Genetics, University of Wisconsin-Madison

Post Doctoral Fellow, Cancer Biology, Fred Hutchinson Cancer Research Center

Education/Training Program Affiliations

Biomedical Science Program, Department of Microbiology Graduate Program, Free Radical and Radiation Biology Graduate Program, Interdisciplinary Graduate Program in Genetics, Interdisciplinary Graduate Program in Informatics, Interdisciplinary Graduate Program in Molecular and Cellular Biology, Interdisciplinary Graduate Program in Translational Biomedicine, Medical Scientist Training Program

Center, Program and Institute Affiliations

Cancer and Aging Program, Center for Bioinformatics and Computational Biology, Center for Gene Therapy of Cystic Fibrosis and other Genetic Diseases, Helen C. Levitt Center for Viral Pathogenesis, Holden Comprehensive Cancer Center

Research Summary

My research interests are in the use of immortalized and primary human cells to build 3D tissues, and to use these human cells and tissues to study microbial and environmental factors that lead to infections, type II diabetes, and cancer. My prior research addressed how human papillomaviruses (HPVs) immortalize and transform epithelial cells, leading to cancer. My laboratory has now extended these studies to a variety of other human cell types. We have developed multiple cell culture model systems to study microbial infections and pathology, as well as to understand how environmental and bacterial factors affect cell physiology to cause disease. For example, we recently initiated collaborative studies to examine how Ebola virus infects and transmits through human skin. Our success with immortalizing human preadipocytes (pre-fat) cells has led to studies on how environmental and bacterial toxins cause or exacerbate diabetes through effects on fat tissue. Working with bioengineers, we are developing 3D systems of cell culture that more closely recapitulate whole tissue, thus moving beyond simple cell culture.

Publications

Klingelhutz, A. J., Gourronc, F. A., Chaly, A., Wadkins, D. A., Burand, A. J., Markan, K. R., Idiga, S. O., Wu, M., Potthoff, M. J. & Ankrum, J. A. (In Press). Scaffold-free generation of uniform adipose spheroids for metabolism research and drug discovery. Scientific Reports, in press.

Scorza, B. M., Wacker, M. A., Messingham, K., Kim, P., Klingelhutz, A., Fairley, J. & Wilson, M. E. (2017). Differential Activation of Human Keratinocytes by Leishmania spp. Causing Localized or Disseminated Disease. J Invest Dermatol, 137(10), 2149-2156. PMID: 28647347.

Kulhankova, K., Kinney, K. J., Stach, J. M., Gourronc, F. A., Grumbach, I. M., Klingelhutz, A. J. & Salgado-Pabón, W. (2017). The Superantigen Toxic Shock Syndrome Toxin-1 Alters Human Aortic Endothelial Cell Function. Infect Immun, Epub ahead of print. PMID: 29229737.

Gourronc, F. A., Robertson, L. W. & Klingelhutz, A. J. (2017). A delayed proinflammatory response of human preadipocytes to PCB126 is dependent on the aryl hydrocarbon receptor. Environ Sci Pollut Res Int, Epub ahead of print. PMID: 28699004.

Jang, J. H., Chand, H. S., Bruse, S., Doyle-Eisele, M., Royer, C., McDonald, J., Qualls, C., Klingelhutz, A. J., Lin, Y., Mallampalli, R., Tesfaigzi, Y. & Nyunoya, T. (2017). Connective Tissue Growth Factor Promotes Pulmonary Epithelial Cell Senescence and Is Associated with COPD Severity. COPD, 14(2), 228-237. PMID: 28026993.

Herrera, A., Kulhankova, K., Sonkar, V. K., Dayal, S., Klingelhutz, A. J., Salgado-Pabón, W. & Schlievert, P. M. (2017). Staphylococcal ß-Toxin Modulates Human Aortic Endothelial Cell and Platelet Function through Sphingomyelinase and Biofilm Ligase Activities. MBio, 8(2), e00273-17. PMID: 28325766.

Zhang, Y., Xie, L., Gunasekar, S. K., Tong, D., Mishra, A., Gibson, W. J., Wang, C., Fidler, T., Marthaler, B., Klingelhutz, A. J., Abel, E. D., Samuel, I., Smith, J. K., Cao, L. & Sah, R. (2017). SWELL1 is a regulator of adipocyte size, insulin signalling and glucose homeostasis. Nat Cell Biol, 19(5), 504-517. PMID: 28436964.

Littlejohn, N. K., Keen, H. L., Weidemann, B. J., Claflin, K. E., Tobin, K. V., Markan, K. R., Park, S., Naber, M. C., Gourronc, F. A., Pearson, N. A., Liu, X., Morgan, D. A., Klingelhutz, A. J., Potthoff, M. J., Rahmouni, K., Sigmund, C. D. & Grobe, J. L. (2016). Suppression of Resting Metabolism by the Angiotensin AT2 Receptor. Cell Rep, 16(6), 1548-60. PMID: 27477281.

Gadupudi, G. S., Klingelhutz, A. J. & Robertson, L. W. (2016). Diminished Phosphorylation of CREB Is a Key Event in the Dysregulation of Gluconeogenesis and Glycogenolysis in PCB126 Hepatotoxicity. Chem Res Toxicol, 29(9), 1504-9. PMID: 27509375.

Gadupudi, G. S., Klaren, W. D., Olivier, A. K., Klingelhutz, A. J. & Robertson, L. W. (2016). PCB126-induced disruption in gluconeogenesis and fatty acid oxidation precedes fatty liver in male rats. Toxicol Sci, 149(1), 98-110. PMID: 26396156.

Vu, B. G., Stach, C. S., Kulhankova, K., Salgado-Pabón, W., Klingelhutz, A. J. & Schlievert, P. M. (2015). Chronic superantigen exposure induces systemic inflammation, elevated bloodstream endotoxin, and abnormal glucose tolerance in rabbits: possible role in diabetes. MBio, 6(2), e02554. PMID: 25714716.

Merriman, J. A., Klingelhutz, A. J., Diekema, D. J., Leung, D. Y. & Schlievert, P. M. (2015). Novel Staphylococcus aureus Secreted Protein Alters Keratinocyte Proliferation and Elicits a Proinflammatory Response In Vitro and In Vivo. Biochemistry, 54(31), 4855-62. PMID: 26177220.

Schlievert, P. M., Salgado-Pabón, W. & Klingelhutz, A. J. (2015). Does Staphylococcus aureus have a role in the development of Type 2 diabetes mellitus?. Future Microbiol, 10(10), 1549-52. PMID: 26439811.

Gadupudi, G., Gourronc, F. A., Ludewig, G., Robertson, L. W. & Klingelhutz, A. J. (2015). PCB126 inhibits adipogenesis of human preadipocytes. Toxicol In Vitro, 29(1), 132-41. PMID: 25304490.

Jang, J. H., Bruse, S., Huneidi, S., Schrader, R. M., Monick, M. M., Lin, Y., Carter, A. B., Klingelhutz, A. J. & Nyunoya, T. (2014). Acrolein-exposed normal human lung fibroblasts in vitro: cellular senescence, enhanced telomere erosion, and degradation of werner's syndrome protein. Environ Health Perspect, 122(9), 955-62. PMID: 24747221.

Hagen, J., Muniz, V. P., Falls, K. C., Reed, S. M., Taghiyev, A. F., Quelle, F. W., Gourronc, F. A., Klingelhutz, A. J., Major, H. J., Askeland, R. W., Sherman, S. K., O'Dorisio, T. M., Bellizzi, A. M., Howe, J. R., Darbro, B. W. & Quelle, D. E. (2014). RABL6A Promotes G1-S Phase Progression and Pancreatic Neuroendocrine Tumor Cell Proliferation in an Rb1-Dependent Manner. Cancer Res, 74(22), 6661-70. PMID: 25273089.

Kimple, R. J., Smith, M. A., Blitzer, G. C., Torres, A. D., Martin, J. A., Yang, R. Z., Peet, C. R., Lorenz, L. D., Nickel, K. P., Klingelhutz, A. J., Lambert, P. F. & Harari, P. M. (2013). Enhanced radiation sensitivity in HPV-positive head and neck cancer. Cancer Res, 73(15), 4791-800. PMID: 23749640.

Vu, B. G., Gourronc, F. A., Bernlohr, D. A., Schlievert, P. M. & Klingelhutz, A. J. (2013). Staphylococcal superantigens stimulate immortalized human adipocytes to produce chemokines. PLoS One, 8(10), e77988. PMID: 24205055.

Hernandez, L. I., Flenker, K. S., Hernandez, F. J., Klingelhutz, A. J., McNamera, J. O. & Giangrande, P. H. (2013). Methods for Evaluating Cell-Specific, Cell-Internalizing RNA Aptamers. Pharmaceuticals (Basel), 6(3), 295-319. PMID: 23894227.

Vande Pol, S. B., Klingelhutz, A. J. (2013). Papillomavirus E6 oncoproteins. Virology, 445(1-2), 115-37. PMID: 23711382.

Pereboeva, L., Westin, E., Patel, T., Flaniken, I., Lamb, L., Klingelhutz, A. J. & Goldman, F. (2013). DNA damage responses and oxidative stress in dyskeratosis congenita. PLoS One, 8(10), e76473. PMID: 24124565.

Gourronc, F. A., Rockey, W. M., Thiel, W. H., Giangrande, P. H. & Klingelhutz, A. J. (2013). Identification of RNA aptamers that internalize into HPV-16 E6/E7 transformed tonsillar epithelial cells. Virology, 446(1-2), 325-33. PMID: 24074596.

Vermeer, P. D., Bell, M., Lee, K., Vermeer, D. W., Wieking, B. G., Bilal, E., Bhanot, G., Drapkin, R. I., Ganesan, S., Klingelhutz, A. J., Hendriks, W. J. & Lee, J. H. (2012). ErbB2, EphrinB1, Src kinase and PTPN13 signaling complex regulates MAP kinase signaling in human cancers. PLoS One, 7(1), e30447. PMID: 22279592.

Gourronc, F. A., Klingelhutz, A. J. (2012). Therapeutic opportunities: telomere maintenance in inducible pluripotent stem cells. Mutat Res, 730(1-2), 98-105. PMID: 21605571.

Buckingham, E. M., Goldman, F. D. & Klingelhutz, A. J. (2012). Dyskeratosis Congenita Dermal Fibroblasts are Defective in Supporting the Clonogenic Growth of Epidermal Keratinocytes. Aging Dis, 3(6), 427-37. PMID: 23251848.

Bulysheva, A. A., Bowlin, G. L., Klingelhutz, A. J. & Yeudall, W. A. (2012). Low-temperature electrospun silk scaffold for in vitro mucosal modeling. J Biomed Mater Res A, 100(3), 757-67. PMID: 22238242.

Klingelhutz, A. J., Roman, A. (2012). Cellular transformation by human papillomaviruses: lessons learned by comparing high- and low-risk viruses. Virology, 424(2), 77-98. PMID: 22284986.

Westin, E. R., Aykin-Burns, N., Buckingham, E. M., Spitz, D. R., Goldman, F. D. & Klingelhutz, A. J. (2011). The p53/p21(WAF/CIP) pathway mediates oxidative stress and senescence in dyskeratosis congenita cells with telomerase insufficiency. Antioxid Redox Signal, 14(6), 985-97. PMID: 21087144.

Saccoccio, F. M., Sauer, A. L., Cui, X., Armstrong, A. E., Habib, e. l., Johnson, D. C., Ryckman, B. J., Klingelhutz, A. J., Adler, S. P. & McVoy, M. A. (2011). Peptides from cytomegalovirus UL130 and UL131 proteins induce high titer antibodies that block viral entry into mucosal epithelial cells. Vaccine, 29(15), 2705-11. PMID: 21310190.

Buckingham, E. M., Klingelhutz, A. J. (2011). The role of telomeres in the ageing of human skin. Exp Dermatol, 20(4), 297-302. PMID: 21371125.

Senthikumar, P. K., Klingelhutz, A. J., Jacobus, J. A., Lehmler, H., Robertson, L. W. & Ludewig, G. (2011). Airborne polychlorinated biphenyls (PCBs) reduce telomerase activity and shorten telomere length in immortal human skin keratinocytes (HaCat). Toxicol Lett, 204(1), 64-70. PMID: 21530622.

Agarwal, S., Loh, Y. H., McLoughlin, E. M., Huang, J., Park, I. H., Miller, J. D., Huo, H., Okuka, M., Dos Reis, R. M., Loewer, S., Ng, H. H., Keefe, D. L., Goldman, F. D., Klingelhutz, A. J., Liu, L. & Daley, G. Q. (2010). Telomere elongation in induced pluripotent stem cells from dyskeratosis congenita patients. Nature, 464(7286), 292-6. PMID: 20164838.

Gourronc, F. A., Robertson, M. M., Herrig, A. K., Lansdorp, P. M., Goldman, F. D. & Klingelhutz, A. J. (2010). Proliferative defects in dyskeratosis congenita skin keratinocytes are corrected by expression of the telomerase reverse transcriptase, TERT, or by activation of endogenous telomerase through expression of papillomavirus E6/E7 or the telomerase RNA component, TERC. Exp Dermatol, 19(3), 279-88. PMID: 19558498.

Nyunoya, T., Monick, M. M., Klingelhutz, A. J., Glaser, H., Cagley, J. R., Brown, C. O., Matsumoto, E., Aykin-Burns, N., Spitz, D. R., Oshima, J. & Hunninghake, G. W. (2009). Cigarette smoke induces cellular senescence via Werner's syndrome protein down-regulation. Am J Respir Crit Care Med, 179(4), 279-87. PMID: 19011155.

Yu, L., Hitchler, M. J., Sun, W., Sarsour, E. H., Goswami, P. C., Klingelhutz, A. J. & Domann, F. E. (2009). AP-2alpha Inhibits c-MYC Induced Oxidative Stress and Apoptosis in HaCaT Human Keratinocytes. J Oncol, 2009, 780874. PMID: 20066163.

Lace, M. J., Anson, J. R., Klingelhutz, A. J., Lee, J. H., Bossler, A. D., Haugen, T. H. & Turek, L. P. (2009). Human papillomavirus (HPV) type 18 induces extended growth in primary human cervical, tonsillar, or foreskin keratinocytes more effectively than other high-risk mucosal HPVs. J Virol, 83(22), 11784-94. PMID: 19740985.

Lace, M. J., Anson, J. R., Klingelhutz, A. J., Harada, H., Taniguchi, T., Bossler, A. D., Haugen, T. H. & Turek, L. P. (2009). Interferon-beta treatment increases human papillomavirus early gene transcription and viral plasmid genome replication by activating interferon regulatory factor (IRF)-1. Carcinogenesis, 30(8), 1336-44. PMID: 19541854.

Hoover, A. C., Strand, G. L., Nowicki, P. N., Anderson, M. E., Vermeer, P. D., Klingelhutz, A. J., Bossler, A. D., Pottala, J. V., Hendriks, W. J. & Lee, J. H. (2009). Impaired PTPN13 phosphatase activity in spontaneous or HPV-induced squamous cell carcinomas potentiates oncogene signaling through the MAP kinase pathway. Oncogene, 28(45), 3960-70. PMID: 19734941.

Spanos, W. C., Geiger, J., Anderson, M. E., Harris, G. F., Bossler, A. D., Smith, R. B., Klingelhutz, A. J. & Lee, J. H. (2008). Deletion of the PDZ motif of HPV16 E6 preventing immortalization and anchorage-independent growth in human tonsil epithelial cells. Head Neck, 30(2), 139-47. PMID: 17657785.

Jacobus, J. A., Flor, S., Klingelhutz, A. J., Robertson, L. W. & Ludewig, G. (2008). 2-(4'-chlorophenyl)-1,4-benzoquinone increases the frequency of micronuclei and shortens telomeres. Environ Toxicol Pharmacol, 25(2), 267-72. PMID: 18438462.

Spanos, W. C., Hoover, A., Harris, G. F., Wu, S., Strand, G. L., Anderson, M. E., Klingelhutz, A. J., Hendriks, W., Bossler, A. D. & Lee, J. H. (2008). The PDZ binding motif of human papillomavirus type 16 E6 induces PTPN13 loss, which allows anchorage-independent growth and synergizes with ras for invasive growth. J Virol, 82(5), 2493-500. PMID: 18160445.

Goldman, F. D., Aubert, G., Klingelhutz, A. J., Hills, M., Cooper, S. R., Hamilton, W. S., Schlueter, A. J., Lambie, K., Eaves, C. J. & Lansdorp, P. M. (2008). Characterization of primitive hematopoietic cells from patients with dyskeratosis congenita. Blood, 111(9), 4523-31. PMID: 18310499.

Westin, E. R., Chavez, E., Lee, K. M., Gourronc, F. A., Riley, S., Lansdorp, P. M., Goldman, F. D. & Klingelhutz, A. J. (2007). Telomere restoration and extension of proliferative lifespan in dyskeratosis congenita fibroblasts. Aging Cell, 6(3), 383-94. PMID: 17381549.

Hoover, A. C., Spanos, W. C., Harris, G. F., Anderson, M. E., Klingelhutz, A. J. & Lee, J. H. (2007). The role of human papillomavirus 16 E6 in anchorage-independent and invasive growth of mouse tonsil epithelium. Arch Otolaryngol Head Neck Surg, 133(5), 495-502. PMID: 17515506.

James, M. A., Lee, J. H. & Klingelhutz, A. J. (2006). Human papillomavirus type 16 E6 activates NF-kappaB, induces cIAP-2 expression, and protects against apoptosis in a PDZ binding motif-dependent manner. J Virol, 80(11), 5301-7. PMID: 16699010.

James, M. A., Lee, J. H. & Klingelhutz, A. J. (2006). HPV16-E6 associated hTERT promoter acetylation is E6AP dependent, increased in later passage cells and enhanced by loss of p300. Int J Cancer, 119(8), 1878-85. PMID: 16708385.

Darbro, B. W., Lee, K. M., Nguyen, N. K., Domann, F. E. & Klingelhutz, A. J. (2006). Methylation of the p16(INK4a) promoter region in telomerase immortalized human keratinocytes co-cultured with feeder cells. Oncogene, 25(56), 7421-33. PMID: 16767161.

Nyunoya, T., Monick, M. M., Klingelhutz, A. J., Yarovinsky, T. O., Cagley, J. R. & Hunninghake, G. W. (2006). Cigarette smoke induces cellular senescence. Am J Respir Cell Mol Biol, 35(6), 681-8. PMID: 16840774.

Berger, K. L., Barriga, F., Lace, M. J., Turek, L. P., Zamba, G. J., Domann, F. E., Lee, J. H. & Klingelhutz, A. J. (2006). Cervical keratinocytes containing stably replicating extrachromosomal HPV-16 are refractory to transformation by oncogenic H-Ras. Virology, 356(1-2), 68-78. PMID: 16945398.

Peterson, M. L., Ault, K., Kremer, M. J., Klingelhutz, A. J., Davis, C. C., Squier, C. A. & Schlievert, P. M. (2005). The innate immune system is activated by stimulation of vaginal epithelial cells with Staphylococcus aureus and toxic shock syndrome toxin 1. Infect Immun, 73(4), 2164-74. PMID: 15784559.

Darbro, B. W., Schneider, G. B. & Klingelhutz, A. J. (2005). Co-regulation of p16INK4A and migratory genes in culture conditions that lead to premature senescence in human keratinocytes. J Invest Dermatol, 125(3), 499-509. PMID: 16117791.

Ault, K. A., Allen, H. K., Phillips, S. L., Zimmerman, M. B. & Klingelhutz, A. J. (2005). Telomerase activity as a potential diagnostic marker for triage of abnormal Pap smears. J Low Genit Tract Dis, 9(2), 93-9. PMID: 15870530.

Klingelhutz, A. J., Qian, Q., Phillips, S. L., Gourronc, F. A., Darbro, B. W. & Patil, S. R. (2005). Amplification of the chromosome 20q region is associated with expression of HPV-16 E7 in human airway and anogenital epithelial cells. Virology, 340(2), 237-44. PMID: 16051300.

Lee, J. H., Yi, S. M., Anderson, M. E., Berger, K. L., Welsh, M. J., Klingelhutz, A. J. & Ozbun, M. A. (2004). Propagation of infectious human papillomavirus type 16 by using an adenovirus and Cre/LoxP mechanism. Proc Natl Acad Sci U S A, 101(7), 2094-9. PMID: 14769917.

Morrison, T. E., Mauser, A., Klingelhutz, A. J. & Kenney, S. C. (2004). Epstein-Barr virus immediate-early protein BZLF1 inhibits tumor necrosis factor alpha-induced signaling and apoptosis by downregulating tumor necrosis factor receptor 1. J Virol, 78(1), 544-9. PMID: 14671137.

Luo, P., Tresini, M., Cristofalo, V., Chen, X., Saulewicz, A., Gray, M. D., Banker, D. E., Klingelhutz, A. J., Ohtsubo, M., Takihara, Y. & Norwood, T. H. (2004). Immortalization in a normal foreskin fibroblast culture following transduction of cyclin A2 or cdk1 genes in retroviral vectors. Exp Cell Res, 294(2), 406-19. PMID: 15023530.

Martin, J. A., Klingelhutz, A. J., Moussavi-Harami, F. & Buckwalter, J. A. (2004). Effects of oxidative damage and telomerase activity on human articular cartilage chondrocyte senescence. J Gerontol A Biol Sci Med Sci, 59(4), 324-37. PMID: 15071075.

Martin, J. A., DeYoung, B. R., Gitelis, S., Weydert, J. A., Klingelhutz, A. J., Kurriger, G. & Buckwalter, J. A. (2004). Telomerase reverse transcriptase subunit expression is associated with chondrosarcoma malignancy. Clin Orthop Relat Res, 426, 117-24. PMID: 15346061.

Landen, C. N., Klingelhutz, A. J., Coffin, J. E., Sorosky, J. I. & Sood, A. K. (2004). Genomic instability is associated with lack of telomerase activation in ovarian cancer. Cancer Biol Ther, 3(12), 1250-3. PMID: 15477760.

Plug-DeMaggio, A. W., Sundsvold, T., Wurscher, M. A., Koop, J. I., Klingelhutz, A. J. & McDougall, J. K. (2004). Telomere erosion and chromosomal instability in cells expressing the HPV oncogene 16E6. Oncogene, 23(20), 3561-71. PMID: 15077181.

Zabner, J., Karp, P., Seiler, M., Phillips, S. L., Mitchell, C. J., Saavedra, M., Welsh, M. & Klingelhutz, A. J. (2003). Development of cystic fibrosis and noncystic fibrosis airway cell lines. Am J Physiol Lung Cell Mol Physiol, 284(5), L844-54. PMID: 12676769.

Palanca-Wessels, M. C., Klingelhutz, A. J., Reid, B. J., Norwood, T. H., Opheim, K. E., Paulson, T. G., Feng, Z. & Rabinovitch, P. S. (2003). Extended lifespan of Barrett's esophagus epithelium transduced with the human telomerase catalytic subunit: a useful in vitro model. Carcinogenesis, 24(7), 1183-90. PMID: 12807723.

Allen, H., Klingelhutz, A. J. (2003). Papillomavirus infection and telomerase activation. Papillomavirus Report, 14(4), 155-162.

Morrison, J. A., Klingelhutz, A. J. & Raab-Traub, N. (2003). Epstein-Barr virus latent membrane protein 2A activates beta-catenin signaling in epithelial cells. J Virol, 77(22), 12276-84. PMID: 14581564.

Duffy, C. L., Phillips, S. L. & Klingelhutz, A. J. (2003). Microarray analysis identifies differentiation-associated genes regulated by human papillomavirus type 16 E6. Virology, 314(1), 196-205. PMID: 14517073.

Sood, A. K., Coffin, J., Jabbari, S., Buller, R. E., Hendrix, M. J. & Klingelhutz, A. J. (2002). p53 null mutations are associated with a telomerase negative phenotype in ovarian carcinoma. Cancer Biol Ther, 1(5), 511-7. PMID: 12496479.

Martin, J. A., Mitchell, C. J., Klingelhutz, A. J. & Buckwalter, J. A. (2002). Effects of telomerase and viral oncogene expression on the in vitro growth of human chondrocytes. J Gerontol A Biol Sci Med Sci, 57(2), B48-53. PMID: 11818423.

Mauser, A., Holley-Guthrie, E., Zanation, A., Yarborough, W., Kaufmann, W., Klingelhutz, A. J., Seaman, W. T. & Kenney, S. (2002). The Epstein-Barr virus immediate-early protein BZLF1 induces expression of E2F-1 and other proteins involved in cell cycle progression in primary keratinocytes and gastric carcinoma cells. J Virol, 76(24), 12543-52. PMID: 12438580.

Martin, J. A., Forest, E., Block, J. A., Klingelhutz, A. J., Whited, B., Gitelis, S., Wilkey, A. & Buckwalter, J. A. (2002). Malignant transformation in human chondrosarcoma cells supported by telomerase activation and tumor suppressor inactivation. Cell Growth Differ, 13(9), 397-407. PMID: 12354749.

Sprague, D. L., Phillips, S. L., Mitchell, C. J., Berger, K. L., Lace, M., Turek, L. P. & Klingelhutz, A. J. (2002). Telomerase activation in cervical keratinocytes containing stably replicating human papillomavirus type 16 episomes. Virology, 301(2), 247-54. PMID: 12359427.

Farwell, D. G., Shera, K. A., Koop, J. I., Bonnet, G. A., Matthews, C. P., Reuther, G. W., Coltrera, M. D., McDougall, J. K. & Klingelhutz, A. J. (2000). Genetic and epigenetic changes in human epithelial cells immortalized by telomerase. Am J Pathol, 156(5), 1537-47. PMID: 10793065.

Klingelhutz, A. J. (1999). The roles of telomeres and telomerase in cellular immortalization and the development of cancer. Anticancer Res, 19(6A), 4823-30. PMID: 10697595.

Kiyono, T., Foster, S. A., Koop, J. I., McDougall, J. K., Galloway, D. A. & Klingelhutz, A. J. (1998). Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature, 396(6706), 84-8. PMID: 9817205.

Anderson, S., Shera, K., Ihle, J., Billman, L., Goff, B., Greer, B., Tamimi, H., McDougall, J. & Klingelhutz, A. J. (1997). Telomerase activation in cervical cancer. Am J Pathol, 151(1), 25-31. PMID: 9212727.

Klingelhutz, A. J. (1997). Telomerase activation and cancer. J Mol Med (Berl), 75(1), 45-9. PMID: 9020383.

Klingelhutz, A. J., Foster, S. A. & McDougall, J. K. (1996). Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature, 380(6569), 79-82. PMID: 8598912.

Klingelhutz, A. J., Hedrick, L., Cho, K. R. & McDougall, J. K. (1995). The DCC gene suppresses the malignant phenotype of transformed human epithelial cells. Oncogene, 10(8), 1581-6. PMID: 7731713.

Klingelhutz, A. J., Barber, S. A., Smith, P. P., Dyer, K. & McDougall, J. K. (1994). Restoration of telomeres in human papillomavirus-immortalized human anogenital epithelial cells. Mol Cell Biol, 14(2), 961-9. PMID: 8289836.

Klingelhutz, A. J., Smith, P. P., Garrett, L. R. & McDougall, J. K. (1993). Alteration of the DCC tumor-suppressor gene in tumorigenic HPV-18 immortalized human keratinocytes transformed by nitrosomethylurea. Oncogene, 8(1), 95-9. PMID: 8380923.

Klingelhutz, A. J., Wu, S. Q., Huang, J. & Reznikoff, C. A. (1992). Loss of 3p13----p21.2 in tumorigenic reversion of a hybrid between isogeneic nontumorigenic and tumorigenic human uroepithelial cells. Cancer Res, 52(6), 1631-4. PMID: 1311637.

Reznikoff, C. A., Kao, C., Bookland, E. A., Klingelhutz, A. J., Pratt, C. I., Wu, S. Q., Gilchrist, K. W. & Swaminathan, S. (1991). Transformation in vitro of human uroepithelial cells. New Jersey: Humana Press.

Wu, S. Q., Storer, B. E., Bookland, E. A., Klingelhutz, A. J., Gilchrist, K. W., Meisner, L. F., Oyasu, R. & Reznikoff, C. A. (1991). Nonrandom chromosome losses in stepwise neoplastic transformation in vitro of human uroepithelial cells. Cancer Res, 51(12), 3323-6. PMID: 2040006.

Klingelhutz, A. J., Wu, S. Q., Bookland, E. A. & Reznikoff, C. A. (1991). Allelic 3p deletions in high-grade carcinomas after transformation in vitro of human uroepithelial cells. Genes Chromosomes Cancer, 3(5), 346-57. PMID: 1686726.

Klingelhutz, A. J., Wu, S. Q. & Reznikoff, C. A. (1991). Nonrandom chromosome losses in tumorigenic revertants of hybrids between isogeneic immortal and neoplastic human uroepithelial cells. Somat Cell Mol Genet, 17(6), 551-65. PMID: 1767334.

Reznikoff, C. A., Bookland, E. A., Klingelhutz, A. J., Pratt, C. I., Kao, C., Bhattacharya, M., Swaminathan, S. & Meisner, L. F. (1989). SV-HUC-1: A human urinary tract epithelial cell line for multistep in vitro transformation studies. England: Adam Hilger Press.