Microproteomic Profiling of High-Grade Squamous Intraepithelial Lesion of the Cervix: Insight into Biological Mechanisms of Dysplasia and New Potential Diagnostic Markers

Pottier, Charles; Kriegsmann, M.; Alberts, D.; Smargiasso, Nicolas; Baiwir, Dominique; Mazzucchelli, Gabriel; Herfs, Michael; Fresnais, M.; Casadonte, R.; Delvenne, Philippe; De Pauw, Edwin; Longuespée, Rémi

doi:10.1002/prca.201800052

Article (Scientific journals)

Microproteomic Profiling of High-Grade Squamous Intraepithelial Lesion of the Cervix: Insight into Biological Mechanisms of Dysplasia and New Potential Diagnostic Markers

Pottier, Charles; Kriegsmann, M.; Alberts, D. et al.

2019 • In Proteomics. Clinical Applications, 13(1)

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/232528

DOI
10.1002/prca.201800052

PubMed
30094940

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Abstract :

[en] Purpose: High-grade squamous intraepithelial lesion (HSIL) is a known precursor for squamous cell carcinoma of uterine cervix. Although it is known that SILs are associated to infection by human papillomavirus, downstream biological mechanisms are still poorly described. In this study, we compared the microproteomic profile of HSIL to normal tissues: ectocervix (ectoC) and endocervix (endoC). Experimental design: Tissue regions of endoC, ectoC, and HSlL were collected by laser microdissection (3500 cells each) from five patients. Samples were processed and analyzed using our recently developed laser microdissection-based microproteomic method. Tissues were compared in order to retrieve HSIL's proteomic profile. Potentially interesting proteins for pathology were stained by immunohistochemistry. Results: We identified 3072 proteins among the fifteen samples and 2386 were quantified in at least four out of the five biological replicates of at least one tissue type. We found 236 proteins more abundant in HSIL. Gene ontology enrichments revealed mechanisms of DNA replication and RNA splicing. Despite the squamous nature of HSIL, a common signature between HSIL and endoC could be found. Finally, potential new markers could support diagnosis of dysplasia in SILs. Conclusion and clinical relevance: This microproteomic investigation of HSIL gives insights into the biology of cervical precancerous lesions. © 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Disciplines :

Oncology

Author, co-author :

Pottier, Charles ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire

Kriegsmann, M.; Institute of pathology, University of Heidelberg, Heidelberg, Germany

Alberts, D.; Mass Spectrometry Laboratory, GIGA-Research, Department of Chemistry, University of Liège, Liège, Belgium

Smargiasso, Nicolas ; Université de Liège - ULiège > Département de chimie (sciences) > Laboratoire de spectrométrie de masse (L.S.M.)

Baiwir, Dominique ; Université de Liège - ULiège > GIGA-Technology platforms : Plate-forme protéomique

Mazzucchelli, Gabriel ; Université de Liège - ULiège > Département de chimie (sciences) > Laboratoire de spectrométrie de masse (L.S.M.)

Herfs, Michael ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Anatomie et cytologie pathologiques

Fresnais, M.; Department of Clinical Pharmacology and Pharmacoepidemiology, University of Heidelberg, Heidelberg, Germany, German Cancer Consortium (DKTK)-German Cancer Research Center (DKFZ), Heidelberg, Germany

Casadonte, R.; Proteopath GmbH, Trier, Germany

Delvenne, Philippe ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Anatomie et cytologie pathologiques

De Pauw, Edwin ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie analytique inorganique

Longuespée, Rémi ; Université de Liège - ULiège > Département de chimie (sciences) > Center for Analytical Research and Technology (CART)

Title :

Microproteomic Profiling of High-Grade Squamous Intraepithelial Lesion of the Cervix: Insight into Biological Mechanisms of Dysplasia and New Potential Diagnostic Markers

Publication date :

2019

Journal title :

Proteomics. Clinical Applications

ISSN :

1862-8346

eISSN :

1862-8354

Publisher :

Wiley-VCH Verlag

Volume :

13(1)

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 04 February 2019

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Bibliography

Wkly. Epidemiol. Rec. 2017, 92, 241.
R. J. Kurman, M. L. Carcangiu, C. S. Herrington, R. H. Young, WHO Classification of Tumours of Female Reproductive Organs, World Health Organization, Geneva, 2014.
M. R. Mccredie, K. J. Sharples, C. Paul, J. Baranyai, G. Medley, R. W. Jones, D. C. Skegg, Lancet. Oncol. 2008, 9, 425.
L. S. Massad, M. H. Einstein, W. K. Huh, H. A. Katki, W. K. Kinney, M. Schiffman, D. Solomon, N. Wentzensen, H. W. Lawson, A. C. G. Conference, J. Lower Genit. Tract Dis. 2013, 17, S1.
D. Chelmow, A. Waxman, J. M. Cain, H. C. Lawrence, 3rd, Obstet. Gynecol. 2012, 119, 695.
J. L. Clark, D. Lu, T. Kalir, Y. Liu, Hum. Pathol. 2016, 55, 51.
G. Kontostathi, J. Zoidakis, N. P. Anagnou, K. I. Pappa, A. Vlahou, M. Makridakis, Expert Rev. Proteomics 2016, 13, 731.
R. Longuespée, D. Alberts, C. Pottier, N. Smargiasso, G. Mazzucchelli, D. Baiwir, M. Kriegsmann, M. Herfs, J. Kriegsmann, P. Delvenne, E. De Pauw, Methods 2016, 104, 154.
R. Longuespée, D. Baiwir, G. Mazzucchelli, N. Smargiasso, E. De Pauw, Methods Mol. Biol. 2018, 1723, 19.
F. A. Tavassoli, P. Devilee, Pathology and Genetics of Tumours of the Breast and Female Genital Organs, World Health Organization, Geneva 2003.
R. Maree, L. Rollus, B. Stevens, R. Hoyoux, G. Louppe, R. Vandaele, J. M. Begon, P. Kainz, P. Geurts, L. Wehenkel, Bioinformatics 2016, 32, 1395.
M. Kriegsmann, A. Harms, D. Kazdal, S. Fischer, A. Stenzinger, J. Leichsenring, R. Penzel, R. Longuespée, K. Kriegsmann, T. Muley, S. Safi, A. Warth, Pathol. Res. Pract. 2018, 214, 408.
E. Ingley, Cell Commun. Signal 2012, 10, 21.
S. Liu, X. Hao, X. Ouyang, X. Dong, Y. Yang, T. Yu, J. Hu, L. Hu, Oncotarget 2016, 7, 75468.
A. Corpet, L. De Koning, J. Toedling, A. Savignoni, F. Berger, C. Lemaitre, R. J. O'sullivan, J. Karlseder, E. Barillot, B. Asselain, X. Sastre-Garau, G. Almouzni, EMBO J. 2011, 30, 480.
J. M. Bailis, S. L. Forsburg, Curr. Opin. Genet. Dev. 2004, 14, 17.
M. Lei, Curr. Cancer Drug Targets 2005, 5, 365.
S. L. Forsburg, Microbiol. Mol. Biol. Rev. 2004, 68, 109.
A. Freeman, L. S. Morris, A. D. Mills, K. Stoeber, R. A. Laskey, G. H. Williams, N. Coleman, Clin. Cancer Res. 1999, 5, 2121.
A. F. Nicol, J. R. Lapa E Silva, C. B. Cunha, S. M. Amaro-Filho, N. Oliveira, B. Grinsztejn, R. K. Friedman, F. Russomano, A. Pires, J. E. Golub, G. J. Nuovo, PLoS One 2012, 7, e32936.
M. Herfs, R. Longuespée, C. M. Quick, P. Roncarati, M. Suarez-Carmona, P. Hubert, A. Lebeau, D. Bruyere, G. Mazzucchelli, N. Smargiasso, D. Baiwir, K. Lai, A. Dunn, F. Obregon, E. J. Yang, E. Pauw, C. P. Crum, P. Delvenne, J. Pathol. 2017, 241, 522.
M. Branca, M. Ciotti, C. Giorgi, D. Santini, L. Di Bonito, S. Costa, A. Benedetto, D. Bonifacio, P. Di Bonito, P. Paba, L. Accardi, S. Syrjanen, C. Favalli, K. Syrjanen, H. P.-P. S. Group, Eur. J. Obstet. Gynecol. Reprod. Biol. 2007, 130, 223.
D. Papini, L. Langemeyer, M. A. Abad, A. Kerr, I. Samejima, P. A. Eyers, A. A. Jeyaprakash, J. M. Higgins, F. A. Barr, W. C. Earnshaw, Nat. Commun. 2015, 6, 7678.
C. Mollinari, C. Reynaud, S. Martineau-Thuillier, S. Monier, S. Kieffer, J. Garin, P. R. Andreassen, A. Boulet, B. Goud, J. P. Kleman, R. L. Margolis, Dev. Cell 2003, 5, 295.
B. Pang, N. Wu, R. Guan, L. Pang, X. Li, S. Li, L. Tang, Y. Guo, J. Chen, D. Sun, H. Sun, J. Dai, J. Bai, G. Ji, P. Liu, A. Liu, Q. Wang, S. Xiao, S. Fu, Y. Jin, Clin. Cancer Res. 2017, 23, 5598.
J. M. Yi, E. J. Kang, H. M. Kwon, J. H. Bae, K. Kang, N. Ahuja, K. Yang, Oncotarget 2017, 8, 26600.
M. Matsuo, C. Nakada, Y. Tsukamoto, T. Noguchi, T. Uchida, N. Hijiya, K. Matsuura, M. Moriyama, Mol. Cancer 2013, 12, 15.
J. Bruun, M. Kolberg, T. C. Ahlquist, E. C. Royrvik, T. Nome, E. Leithe, G. E. Lind, M. A. Merok, T. O. Rognum, G. Bjorkoy, T. Johansen, A. Lindblom, X. F. Sun, A. Svindland, K. Liestol, A. Nesbakken, R. I. Skotheim, R. A. Lothe, Clin. Cancer Res. 2015, 21, 3759.
N. Sen, B. Gui, R. Kumar, Cancer Metastasis Rev. 2014, 33, 869.
B. Zhang, H. Zhang, G. Shen, Jpn. J. Clin. Oncol. 2015, 45, 755.
M. Wu, X. Ye, X. Deng, Y. Wu, X. Li, L. Zhang, Onco. Targets Ther. 2016, 9, 1647.
F. Z. Wei, Z. Cao, X. Wang, H. Wang, M. Y. Cai, T. Li, N. Hattori, D. Wang, Y. Du, B. Song, L. L. Cao, C. Shen, L. Wang, H. Wang, Y. Yang, D. Xie, F. Wang, T. Ushijima, Y. Zhao, W. G. Zhu, Autophagy 2015, 11, 2309.
W. Ding, W. Hu, H. Yang, T. Ying, Y. Tian, Int. J. Clin. Exp. Pathol. 2015, 8, 7173.
H. X. Wang, Y. Tan, Zhonghua Yi Xue Za Zhi 2010, 90, 61.
J. Fang, H. Wang, W. Xi, G. Cheng, S. Wang, S. Su, S. Zhang, Y. Deng, Z. Song, A. Xu, B. Liu, J. Cao, Z. Wang, Tumour. Biol. 2015, 36, 5209.
I. M. Sonderstrup, S. B. Nygard, T. S. Poulsen, D. Linnemann, J. Stenvang, H. J. Nielsen, J. Bartek, N. Brunner, P. Norgaard, L. Riis, Mol. Oncol. 2015, 9, 1207.
M. Grunnet, D. Calatayud, N. A. Schultz, J. P. Hasselby, M. Mau-Sorensen, N. Brunner, J. Stenvang, Scand. J. Gastroenterol. 2015, 50, 485.
M. Li, Y. Liu, Genomics Proteomics Bioinformatics 2016, 14, 166.
Y. C. Lee, C. H. Lee, H. P. Tsai, H. W. An, C. M. Lee, J. C. Wu, C. S. Chen, S. H. Huang, J. Hwang, K. T. Cheng, P. L. Leiw, C. L. Chen, C. M. Lin, PLoS One 2015, 10, e0132579.
I. Ugrinova, I. G. Pashev, E. A. Pasheva, Biochemistry 2009, 48, 6502.
N. Syed, S. Chavan, N. A. Sahasrabuddhe, S. Renuse, G. Sathe, V. Nanjappa, A. Radhakrishnan, R. Raja, S. M. Pinto, A. Srinivasan, T. S. Prasad, K. Srikumar, H. Gowda, V. Santosh, D. Sidransky, J. A. Califano, A. Pandey, A. Chatterjee, Proteomics 2015, 15, 383.
A. Sharma, R. Ray, M. R. Rajeswari, Cancer Invest. 2008, 26, 843.
Y. Wang, X. P. Li, J. Y. Yin, Y. Zhang, H. He, C. Y. Qian, J. Chen, Y. Zheng, K. Smieszkol, Y. L. Fu, Z. Y. Chen, H. H. Zhou, Z. Q. Liu, Clin. Exp. Pharmacol. Physiol. 2014, 41, 408.
Z. B. Wu, L. Cai, S. J. Lin, Z. K. Xiong, J. L. Lu, Y. Mao, Y. Yao, L. F. Zhou, Neuro. Oncol. 2013, 15, 1264.
R. R. Varma, S. M. Hector, K. Clark, W. R. Greco, L. Hawthorn, L. Pendyala, Oncol. Rep. 2005, 14, 925.
Y. An, Z. Zhang, Y. Shang, X. Jiang, J. Dong, P. Yu, Y. Nie, Q. Zhao, Cell Death Dis. 2015, 6, e1766.
M. K. Hassumi-Fukasawa, F. A. Miranda-Camargo, B. R. Zanetti, D. F. Galano, A. Ribeiro-Silva, E. G. Soares, Pathol. Oncol. Res. 2012, 18, 929.
C. Kunos, W. Deng, D. Dawson, J. S. Lea, K. M. Zanotti, H. J. Gray, D. P. Bender, P. P. Guaglianone, J. S. Carter, K. N. Moore, Int. J. Gynecol. Cancer 2015, 25, 484.
S. A. Lajud, D. A. Nagda, T. Yamashita, J. Zheng, N. Tanaka, W. M. Abuzeid, A. Civantos, O. Bezpalko, B. W. O'malley Jr., D. Li, Clinl. Cancer Res. 2014, 20, 6465.
B. Altan, T. Yokobori, M. Ide, T. Bai, T. Yanoma, A. Kimura, N. Kogure, M. Suzuki, P. Bao, E. Mochiki, K. Ogata, T. Handa, K. Kaira, M. Nishiyama, T. Asao, T. Oyama, H. Kuwano, Anticancer Res. 2016, 36, 5237.
B. Q. Yi, B. Zhao, Z. J. Wang, Hepatogastroenterology 2011, 58, 785.
S. Deb, H. Xu, J. Tuynman, J. George, Y. Yan, J. Li, R. L. Ward, N. Mortensen, N. J. Hawkins, M. J. Mckay, R. G. Ramsay, S. B. Fox, Br. J. Cancer 2014, 110, 1606.
H. Xu, M. Yan, J. Patra, R. Natrajan, Y. Yan, S. Swagemakers, J. M. Tomaszewski, S. Verschoor, E. K. Millar, P. Van Der Spek, J. S. Reis-Filho, R. G. Ramsay, S. A. O'toole, C. M. Mcneil, R. L. Sutherland, M. J. Mckay, S. B. Fox, Breast Cancer Res. 2011, 13, R9.
E. R. Nijhuis, H. W. Nijman, K. A. Oien, A. Bell, K. A. Ten Hoor, N. Reesink-Peters, H. M. Boezen, H. Hollema, A. G. Van Der Zee, J. Clin. Pathol. 2007, 60, 824.
B. Azzimonti, M. Pagano, M. Mondini, M. De Andrea, G. Valente, G. Monga, M. Tommasino, P. Aluffi, S. Landolfo, M. Gariglio, Histopathology 2004, 45, 560.
M. K. Jang, D. E. Anderson, K. Van Doorslaer, A. A. Mcbride, Proteomics 2015, 15, 2038.
M. Le Gallo, A. J. O'hara, M. L. Rudd, M. E. Urick, N. F. Hansen, N. J. O'neil, J. C. Price, S. Zhang, B. M. England, A. K. Godwin, D. C. Sgroi, N. I. H. I. S. C. C. S. Program, P. Hieter, J. C. Mullikin, M. J. Merino, D. W. Bell, Nat. Genet. 2012, 44, 1310.
M. R. Pan, H. J. Hsieh, H. Dai, W. C. Hung, K. Li, G. Peng, S. Y. Lin, J. Biol. Chem. 2012, 287, 6764.
J. L. Slack, K. Schooley, T. P. Bonnert, J. L. Mitcham, E. E. Qwarnstrom, J. E. Sims, S. K. Dower, J. Biol. Chem. 2000, 275, 4670.
N. C. Di Paolo, D. M. Shayakhmetov, Nat. Immunol. 2016, 17, 906.
A. M. Lewis, S. Varghese, H. Xu, H. R. Alexander, J. Transl. Med. 2006, 4, 48.
S. Wawrocki, M. Druszczynska, M. Kowalewicz-Kulbat, W. Rudnicka, Acta. Biochim. Pol. 2016, 63, 59.
M. Herfs, Y. Yamamoto, A. Laury, X. Wang, M. R. Nucci, M. E. Mclaughlin-Drubin, K. Munger, S. Feldman, F. D. Mckeon, W. Xian, C. P. Crum, PNAS 2012, 109, 10516.
H. Lee, H. Lee, Y. K. Cho, Diagn. Pathol. 2017, 12, 18.
M. Herfs, C. Parra-Herran, B. E. Howitt, A. R. Laury, M. R. Nucci, S. Feldman, C. A. Jimenez, F. D. Mckeon, W. Xian, C. P. Crum, Am. J. Surg. Pathol. 2013, 37, 1311.
A. Lopez-Ferrer, F. Alameda, C. Barranco, M. Garrido, C. De Bolos, Hum. Pathol. 2001, 32, 1197.
E. G. Munro, M. Jain, E. Oliva, N. Kamal, S. M. Lele, M. P. Lynch, L. Guo, K. Fu, P. Sharma, S. Remmenga, W. B. Growdon, J. S. Davis, B. R. Rueda, S. K. Batra, Int. J. Gynecol. Pathol. 2009, 28, 127.
H. Griffin, Y. Soneji, R. Van Baars, R. Arora, D. Jenkins, M. Van De Sandt, Z. Wu, W. Quint, R. Jach, K. Okon, H. Huras, A. Singer, J. Doorbar, Mod. Pathol. 2015, 28, 977.
R. Longuespée, M. Fléron, C. Pottier, F. Quesada-Calvo, M. A. Meuwis, D. Baiwir, N. Smargiasso, G. Mazzucchelli, M. C. De Pauw-Gillet, P. Delvenne, E. De Pauw, OMICS 2014, 18, 539.
E. Y. Chen, A. Tran, C. J. Raho, C. M. Birch, C. P. Crum, M. S. Hirsch, Mod. Pathol. 2010, 23, 1045.