Research Summary

My research focus is investigation of the interactions of human viruses, including human cytomegalovirus (HCMV), Epstein–Barr virus (EBV), Herpes simplex virus (HSV), human immunodeficiency virus (HIV), and human papillomavirus (HPV), with monostratified and multistratified oral epithelia. We have made significant contributions to current knowledge about entry, transcytosis, intracellular transport, egress, and cell-to-cell transmission of these viruses in oral epithelial cells by establishing and using polarized epithelial cells, as well as ex vivo oral mucosal tissue explants. Currently, we are investigating the potential interactions of HIV with other viral pathogens, including human papillomavirus HPV. The incidence of HPV-associated oral cancer in human immunodeficiency virus (HIV)-positive individuals is substantially higher than in HIV-uninfected individuals. Our data show that oral epithelial biopsies from HIV-infected individuals and oral keratinocytes grown in tissue culture from HIV-infected individuals have multiple changes consistent with epithelial-mesenchymal transition (EMT), a multistep epigenetic process characterized by loss of cell adhesion and increased proliferation and mobility of epithelial cells. EMT is important in cell differentiation during embryogenesis. However, it is also plays a critical role in progression of neoplastic processes. We expect that our research may led to better understanding the role of HIV-associated EMT in development of HPV-associated neoplasia.

Research Funding

  • December 1, 2018 - November 30, 2023 - Role of HIV in acceleration of HPV malignancy, Principal Investigator. Sponsor: NIH/NCI, Sponsor Award ID: R01CA232887
  • September 6, 2018 - June 30, 2023 - Role of oral herpesvirus microbiota in pathogenesis of HIV mother to child transmission, Principal Investigator. Sponsor: NIH/NIDCR, Sponsor Award ID: R01DE028129
  • May 1, 2013 - March 31, 2018 - Molecular mechanisms of oral HIV transmission modeling MTCT, Principal Investigator. Sponsor: NIH/NIDCR, Sponsor Award ID: R01DE023315
  • July 2, 2010 - June 30, 2013 - HIV transcellular and transsynaptic penetration of mucosal epithelium, Principal Investigator. Sponsor: NIH/NIDCR, Sponsor Award ID: R21DE021011

Education

Institute of Agriculture, School of Veterinary Medicine, Samarkand, Uzbekistan (former Soviet Union), DVM 1981, Veterinary Medicine
Institute of Experimental Veterinary Medicine and Ivanosky Institute of Virology, Moscow, Russia, PhD, 1985, Virology, Cell Biology
Ivanosky Institute of Virology, Russian Academy of Medical Sciences, Moscow, Russia, DSc, 1996, Medical Virology Infectious Disease

Selected Publications

  1. Tugizov SM Human immunodeficiency virus interaction with oral and genital mucosal epithelia may lead to epithelial-mesenchymal transition and sequestration of virions in the endosomal compartments.  View on PubMed
  2. Weinberg A, Tugizov S, Pandiyan P, Jin G, Rakshit S, Vyakarnam A, Naglik JR Innate immune mechanisms to oral pathogens in oral mucosa of HIV-infected individuals.  View on PubMed
  3. Lien K, Mayer W, Herrera R, Rosbe K, Tugizov SM HIV-1 proteins gp120 and tat induce the epithelial-mesenchymal transition in oral and genital mucosal epithelial cells.  View on PubMed
  4. Walhart T, Isaacson-Wechsler E, Ang KH, Arkin M, Tugizov S, Palefsky JM A Cell-Based Renilla Luminescence Reporter Plasmid Assay for High-Throughput Screening to Identify Novel FDA-Approved Drug Inhibitors of HPV-16 Infection.  View on PubMed
  5. Wechsler EI, Tugizov S, Herrera R, Costa MD, Palefsky JM Erratum: E5 can be expressed in anal cancer and leads to epidermal growth factor receptor-induced invasion in a human papillomavirus 16-transformed anal epithelial cell line.  View on PubMed
  6. Sufiawati I, Tugizov SM HIV-induced matrix metalloproteinase-9 activation through mitogen-activated protein kinase signalling promotes HSV-1 cell-to-cell spread in oral epithelial cells.  View on PubMed
  7. Wechsler EI, Tugizov S, Herrera R, Da Costa M, Palefsky JM E5 can be expressed in anal cancer and leads to epidermal growth factor receptor-induced invasion in a human papillomavirus 16-transformed anal epithelial cell line.  View on PubMed
  8. Yasen A, Herrera R, Rosbe K, Lien K, Tugizov SM HIV internalization into oral and genital epithelial cells by endocytosis and macropinocytosis leads to viral sequestration in the vesicles.  View on PubMed
  9. Yasen A, Herrera R, Rosbe K, Lien K, Tugizov SM Release of HIV-1 sequestered in the vesicles of oral and genital mucosal epithelial cells by epithelial-lymphocyte interaction.  View on PubMed
  10. Haga T, Efird JT, Tugizov S, Palefsky JM Increased TNF-alpha and sTNFR2 levels are associated with high-grade anal squamous intraepithelial lesions in HIV-positive patients with low CD4 level.  View on PubMed
  11. Tugizov S Human immunodeficiency virus-associated disruption of mucosal barriers and its role in HIV transmission and pathogenesis of HIV/AIDS disease.  View on PubMed
  12. Herrera R, Morris M, Rosbe K, Feng Z, Weinberg A, Tugizov S Human beta-defensins 2 and -3 cointernalize with human immunodeficiency virus via heparan sulfate proteoglycans and reduce infectivity of intracellular virions in tonsil epithelial cells.  View on PubMed
  13. Sufiawati I, Tugizov SM HIV-associated disruption of tight and adherens junctions of oral epithelial cells facilitates HSV-1 infection and spread.  View on PubMed
  14. Tugizov SM, Herrera R, Chin-Hong P, Veluppillai P, Greenspan D, Michael Berry J, Pilcher CD, Shiboski CH, Jay N, Rubin M, Chein A, Palefsky JM HIV-associated disruption of mucosal epithelium facilitates paracellular penetration by human papillomavirus.  View on PubMed
  15. Tugizov SM, Herrera R, Palefsky JM Epstein-Barr virus transcytosis through polarized oral epithelial cells.  View on PubMed
  16. Sharof M. Tugizov, Rossana Herrera, Piri Veluppillai, Deborah Greenspan, Joel M. Palefsky 46. HIV-induced epithelial–mesenchymal transition in mucosal epithelium facilitates HPV paracellular penetration.  View on PubMed
  17. Erin Isaacson Wechsler, Sharof Tugizov, Joel Palefsky 48. Cidofovir treatment prevents invasion of invasive HPV-16-positive anal keratinocytes.  View on PubMed
  18. . Sargeant, S. Deverasetty, Y. Luo, A. Villahoz-Baleta, S. Zobrist, V. Rathnayake, J. Russo, M. Muesing, M. Schiller, R. Andrabi, R. Kumar, M. Bala, A. Nair, A. Biswas, N. Wig, P. Kumar, K. Luthra, N. Gonzalez, K. McKee, E. Yuste, J.R. Mascola, J. Alcamí, L. Vojnov, M. Martins, A. Bean, M. Veloso de Santana, J. Sacha, N. Wilson, M. Bonaldo, R. Galler, M. Stevenson, D. Watkins, M. Aziz, M. Mata, F. Mahmood, H. Durkin, C. Liu, R. Greenblatt, M. Nowicki, E. Golub, K. Anastos, A. French, L. Baum, V.S. Wacleche, N. Chomont, A. Gosselin, P. Monteiro, M. Goupil, H. Kared, C. Tremblay, N. Bernard, M.-R. Boulassel, J.-P. Routy, P. Ancuta, J. Jadlowsky, C. Baiduc, M. Richardson, A. Bennett, B. Jakobsen, J.L. Riley, B. Vingert, D. Benati, O. Lambotte, P. de Truchis, L. Slama, P. Jeannin, S. Perez-Patrigeon, F. Boufassa, W.W. Kwok, F. Lemaître, J.-F. Delfraissy, J. Thèze, L.A. Chakrabarti, M. French, R. Center, K. Wilson, I. Fleyfel, S. Fernandez, A. Kelleher, P. An, J. Goedert, S. Donfield, S. Buchbinder, G. Kirk, R. Detels, C. Winkler, J. Lajoie, J. Juno, A. Burgener, S. Rahman, K. Mogk, C. Wachihi, J. Mwanjewe, F.A. Plummer, J. Kimani, T.B. Ball, K.R. Fowke, A. Burgener, J. Lajoie, C. Wachihi, J. Kimani, K. Fowke, F.A. Plummer, T.B. Ball, T.N. Dieye, A. Chentouffi, M. Camara, S. Sarr, M.V. Tran, M. Seydi, G. Dasgupta, M. Fall, G. Daneau, P.A. Diaw, L. Kestens, P.S. Sow, S. Mboup, L. Benmohamed, D.M. Asmuth, Z.-M. Ma, A. Albanese, S. Devaraj, E. Hodzic, J.-C. Garcia, T.H. Knight, N.M. Flynn, S. Mann, T. Yotter, E. Tsuchida, C.J. Miller, S. Pallikkuth, L. Micci, Z. Ende, R. Iriele, B. Cervasi, J. Else, G. Silvestri, F. Villinger, S. Pahwa, M. Paiardini, S. Solomon, K.G. Murugavel, R. Vignesh, D. Bella, R. Shoba, S. Poongulali, N. Kumarasamy, A. Landay, S.S. Solomon, C.R. Swathirajan, P. Balakrishnan, S. Cu-Uvin, K.H. Mayer, B.L. Shacklett, C.S. Palmer, J. Zhou, S. Saleh, L. Lam, A. Hearps, A. Maisa, C. Pereira, S. Lewin, A. Jaworowski, J.M. McCune, S. Crowe, G. Doitsh, N. Galloway, K. Monroe, Z. Yang, O. Zepeda, W.C. Greene, M. Patel, M.-A. Jenabian, B. Lebouché, M.-J. Brouillette, C. Tremblay, I. Kema, M.-R. Boulassel, J.-P. Routy, F. Al-Ghazawi, E. Faller, P. Parmar, J. Kakal, P. MacPherson, F. Al-Ghazawi, P. Parmar, E. Faller, S. Sugden, N. Sant, P. MacPherson, C. Vinton, J. Brenchley, B. Tabb, X.P. Hao, V.M. Hirsch, M. Paiardini, J. Lifson, G. Silvestri, J.D. Estes, F. Bushman, S. Sherrill-Mix, K. Ocwieja, R. Mukherjee, M. Brown, J. Chin, R. Custers-Allen, P. David, J. Olson, K. Travers, E. Schadt, M. Sánchez del Cojo, M.R. López-Huertas, E. Mateos, M. Coiras, J. Alcamí, G. Sampey, R. Van Duyne, I. Guendel, E. Gregg, N. Shafagati, M. Tyagi, R. Easely, Z. Klase, F. Romerio, M. Iglesias-Ussel, S. Nekhai, K. Kehn-Hall, F. Kashanchi, N. Kumar, V. Evans, S. Saleh, C.F. Pereira, P. Ellenberg, P.U. Cameron, S.R. Lewin, L. Gray, D. Cowley, E. Crespan, C. Welsh, C. Mackenzie, P. Gorry, S. Wesselingh, M. Churchill, M. Iglesias-Ussel, L. Marchionni, F. Romerio, S. Weber, H. Burger, K. Kemal, B. Weiser, K. Korn, K. Anastos, W. Doerfler, S. Saleh, D. Vatakis, P. Cameron, A. Harman, A. Cunningham, S. Lewin, D. Ma, A. Cillo, C.L. Xu, J. Kristoff, J. Fang, G. Haret-Richter, J. Mellors, I. Pandrea, C. Apetrei, B. Trinité, E. Ohlson, S. Rana, J. Alster, D.N. Levy, A.F.B. Victoriano, Y. Hibi, N. Tan Gana, K. Asamitsu, T. Okamoto, M. Marsden, M. Kovochich, N. Suree, S. Shimizu, R. Mehta, R. Cortado, G. Bristol, D.S. An, J. Zack, N. Madrid-Elena, B. Hernandez-Novoa, M. Lamas, L. Garcia-Bermejo, S. Moreno, T. Ruel, J. Achan, W. Huang, H. Cao, P. Li, L.A. Eller, M. Killian, E. Sinclair, E. Charlebois, D.V. Havlir, J. Wong, T.J. Henrich, G. Sciaranghella, J.Z. Li, S. Gallien, V. Ho, A.S. Lacasce, D.R. Kuritzkes, J. Lifson, G. Del Prete, R. Kiser, C.M. Trubey, J. Smedley, V. Coalter, K. Oswald, R. Shoemaker, R. Fast, Y. Li, A. Lara, A. Wiles, R. Wiles, R. Macallister, R. Sanchez, J. Wai, C. Tan, B. Keele, J. Estes, M. Piatakjr, D. Hazuda, J. Symons, S. Deeks Track A Basic Science.  View on PubMed
  19. Tugizov SM, Herrera R, Veluppillai P, Greenspan D, Soros V, Greene WC, Levy JA, Palefsky JM Differential transmission of HIV traversing fetal oral/intestinal epithelia and adult oral epithelia.  View on PubMed
  20. Challacombe SJ, Fidel PL, Tugizov S, Tao L, Wahl SM HIV infection and specific mucosal immunity: workshop 4B.  View on PubMed

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