19th Ave New York, NY 95822, USA

Molecular Oncology Group

Molecular Oncology Group

VHIO’s Molecular Oncology Group applies state-of-the-art tissue-based technologies to basic, translational, and clinical research with a clear focus on developing and validating novel tumor biomarkers for precision medicine in oncology.

Together with VHIO’s Cancer Genomics Group and Oncology Data Science – ODysSey Group, we participate in our in-house Molecular Prescreening Program. We molecularly profile over 1,500 patients per year as candidates for enrolment in early phase clinical trials at our Research Unit for Molecular Therapy of Cancer (UITM) – CaixaResearch.

Our group also serves as one of VHIO’s Core Technology Platforms and our laboratory is therefore key to VHIO’s translational research lines and programs. We actively participate in all projects involving the use of human tissue collected from patients, including biomarker analyses for patient stratification and inclusion in clinical trials, digital pathology, tissue banking and the development of primary patient-derived xenograft (PDX) models.

Our team also continues to work both independently as well as in partnership to establish the impact of microbiome in colorectal cancer development and progression. In particular, we developed a Fusobacterium nucleatum diagnostic assay that permits the simultaneous visualization and quantification of bacteria within tumors. Using this assay we identified, for the very first time, Fusobacterium nucleatum as a biomarker of relapse in rectal cancer (Annals of Oncology 2020). We are also leading the FUSOMAP, a 3-year project funded by the Mutua Madrileña Foundation and Instituto de Salud Carlos III – ISCIII (Institute of Health Carlos III), to develop microbiota-based diagnostic and prognostic models by mapping intratumoral Fusobacterium and associated gut microbiota in early-stage colorectal cancer.

Paolo G. Nuciforo
Group Leader
  • Discovery and validation of novel biomarkers using tissue-based technologies.
  • Identification of targetable alterations as part of VHIO’s Molecular Prescreening Program
  • Application of molecular pathology strategies to support early clinical drug development programs.
  • Resolve spatial interaction of tumor-associated microbiota, tumor cells, and immune cells in the tumor microenvironment.
  • Multiplexed immunohistochemistry and digital image analysis for high-resolution, single cell, tissue biomarker contexture analyses.
  • Better define molecular target epidemiology to render treatment strategies more precise.
  • Act as a central and local laboratory in clinical trials.
  • Serve as a Core Facility for VHIO research programs.

Figure: A) KiQuant workflow. B) A tumor core sequentially stained with Ki67 (top) and Pan-Keratin (middle). The two stainings are aligned into a single virtual digital image (bottom). Tumor region of interest are automatically identified by the Pan-Keratin-positive brown areas (dotted orange line). Green and red cells represent Ki67-negative and -positive nuclei, respectively.

Molecular Oncology Group
Group Leader
Paolo G. Nuciforo
Attending Physicians
Roberta Fasani
Sara Simonetti
Laboratory Supervisor
Jose Antonio Jiménez
Laboratory Assistant
Mª Ángeles Diaz
Post-Doctoral Fellow
Francisca Gallego
PhD Students
Garazi Serna
Stefania Napoli
Image analyst
Eloy Garcia
Technicians
Lidia Alonso
Eloy Garcia
Xavier Guardia
Paola Martinez
Lidia Sánchez
Gertrudis Sánchez
César Sevillano
Student
Ana Santamaria Lacuesta

Most relevant scientific publications

  • Immune microenvironment characterisation and dynamics during anti-HER2-based neoadjuvant treatment in HER2-positive breast cancer. Griguolo G, Serna G, Pascual T, Fasani R, Guardia X, Chic N, Paré L, Pernas S, Muñoz M, Oliveira M, Vidal M, Llombart-Cussac A, Cortés J, Galván P, Bermejo B, Martínez N, López R, Morales S, Garau I, Manso L, Alarcón J, Martínez E, Villagrasa P, Prat A, Nuciforo P.NPJ Precis Oncol. 2021 Mar 19;5(1):23. doi: 10.1038/s41698-021-00163-6.
  • Severe SARS-CoV-2 placenta infection can impact neonatal outcome in the absence of vertical transmission. Cribiù FM, Erra R, Pugni L, Rubio-Perez C, Alonso L, Simonetti S, Croci GA, Serna G, Ronchi A, Pietrasanta C, Lunghi G, Fagnani AM, Piñana M, Matter M, Tzankov A, Terracciano L, Anton A, Ferrazzi E, Ferrero S, Iurlaro E, Seoane J, Nuciforo P.J Clin Invest. 2021 Mar 15;131(6):e145427. doi: 10.1172/JCI145427.
  • Serna G, Ruiz-Pace F, Hernando J, Alonso L, Fasani R, Landolfi S, Comas R, Jimenez J, Elez E, Bullman S, Tabernero J, Capdevila J, Dienstmann R, Nuciforo P. Fusobacterium nucleatum persistence and risk of recurrence after preoperative treatment in locally advanced rectal cancer. Ann Oncol. 2020 Oct;31(10):1366-1375.
  • Serna G, Simonetti S, Fasani R, Pagliuca F, Guardia X, Gallego P, Jimenez J, Peg V, Saura C, Eppenberger-Castori S, Ramon Y Cajal S, Terracciano L, Nuciforo P. Sequential immunohistochemistry and virtual image reconstruction using a single slide for quantitative KI67 measurement in breast cancer. Breast. 2020 Oct;53:102-110.
  • Dienstmann R, Garralda E, Aguilar S, Sala G, Viaplana C, Ruiz-Pace F, González- Zorelle J, Grazia LoGiacco D, Ogbah Z, Ramos Masdeu L, Mancuso F, Fasani R, Jimenez J, Martinez P, Oaknin A, Saura C, Oliveira M, Balmaña J, Carles J, Macarulla T, Elez E, Alsina M, Braña I, Felip E, Tabernero J, Rodon J, Nuciforo P, Vivancos A. Evolving Landscape of Molecular Prescreening Strategies for Oncology Early Clinical Trials. JCO Precis Oncol. 2020 May 14;4:PO.19.00398.
  • Capdevila J, Mayor R, Mancuso FM, Iglesias C, Caratú G, Matos I, Zafón C, Hernando J, Petit A, Nuciforo P, Cameselle-Teijeiro JM, Álvarez CV, Recio JA, Tabernero J, Matias-Guiu X, Vivancos A, Seoane J. Early evolutionary divergence between papillary and anaplastic thyroid cancers. Ann Oncol. 2019 Nov 1;30(11):1843.
  • Vivancos A, Élez E, Salazar R. Circulating cell-free DNA as predictor of treatment failure after neoadjuvant chemoradiotherapy before surgery in patients with locally advanced rectal cancer: is it ready for primetime? Ann Oncol.29: 532-534.
  • Capdevila J,Mayor R; Mancuso FF, Iglesias C; Caratù G, Matos I, Zafón C, Hernando J, Petit A, Nuciforo P, Cameselle-Teijeiro JM, Álvarez C, Recio JA, Tabernero J, Matias-Guiu X, Vivancos A, Seoane J. Early evolutionary divergence between papillary and anaplastic thyroid cancers. Ann Oncol.29: 1454-1460.
  • Cedrés S, Felip E, Cruz C, Martinez de Castro A, Pardo N, Navarro A, Martinez-Marti A, Remon J, Zeron-Medina J, Balmaña J, Llop-Guevara A, Miquel JM, Sansano I, Nuciforo P,Mancuso F, Serra V, Vivancos A. Activity of HSP90 Inhibiton in a Metastatic Lung Cancer Patient With a Germline BRCA1 Mutation. J Natl Cancer Inst.110: 914-917.
  • Puig I, Tenbaum SP, Chicote I, Arqués O,Martínez-Quintanilla J, Cuesta-Borrás E, Ramírez L, Gonzalo P, Soto A, Aguilar S, Eguizabal C, Caratù G, Prat A, Argilés G, Landolfi S, Casanovas O, Serra V, Villanueva A, Arroyo AG, Terracciano L, Nuciforo P,Seoane J,Recio JA, Vivancos A,Dienstmann R,Tabernero J,Palmer HG.TET2 controls chemoresistant slow-cycling cancer cell survival and tumor recurrence. J Clin Invest.128: 3887-3905.
  • Cruz C, Castroviejo-Bermejo M, Gutiérrez-Enríquez S,Llop-Guevara A, Ibrahim YH, Gris-Oliver A, Bonache S, Morancho B, Bruna A, Rueda OM, Lai Z, Polanska UM, Jones GN; Kristel P, de Bustos L, Guzman M,Rodriguez O, Grueso J, Montalban G, Caratú G,Mancuso F, Fasani R, Jiménez J, Howat WJ, Dougherty B, Vivancos A, Nuciforo P, Serres-Créixams X, Rubio IT, Oaknin A, Cadogan E, Barrett JC, Caldas C, Baselga J, Saura C, Cortés J, Arribas J, Jonkers J, Díez O; O’Connor MJ, Balmaña J,Serra V. RAD51 foci as a functional biomarker of homologous recombination repair and PARP inhibitor resistance in germline BRCA-mutated breast cancer. Ann Oncol.29: 1203-1210. IF: 13,926
  • Martínez-Ricarte F, Mayor R, Martínez-Sáez E, Rubio-Pérez C, Pineda E, Cordero E, Cicuéndez M, Poca MA, Lopez-Bigas N, Ramón Y Cajal S, Vieito M, Carles J, Tabernero J,Vivancos A, Gallego S, Graus F, Sahuquillo J, Seoane J. Molecular Diagnosis of Diffuse Gliomas through Sequencing of Cell-Free Circulating Tumor DNA from Cerebrospinal Fluid.Clin Cancer Res.24: 2812-2819.

All publications

  • Chic, Nuria ; Luen, Stephen J ; NUCIFORO, PAOLO GIOVANNI; Salgado, Roberto ; Fumagalli, Debora ; Hilbers, Florentine ; Wang, Yingbo ; de Azambuja, Evandro ; Làng, István ; DI COSIMO, SERENA; SAURA MANICH, CRISTINA; Huober, Jens ; PRAT APARICIO, ALEIX; Loi, Sherene. Tumor Cellularity and Infiltrating Lymphocytes (CelTIL) as a Survival Surrogate in HER2-Positive Breast Cancer. JNCI-JOURNAL OF THE NATIONAL CANCER INSTITUTE.1093/jnci/djab057
  • Frigola, Joan; NAVARRO MENDIVIL, ALEJANDRO; Carbonell, Caterina ; Callejo, Ana ; Iranzo, Patricia ; CEDRES PEREZ, SUSANA; MARTINEZ MARTI, ALEXANDRE; PARDO ARANDA, NURIA; Saoudi-Gonzalez, Nadia ; Martinez, Debora ; JIMENEZ, JOSE; Sansano, Irene ; MANCUSO, FRANCESCO MATTIA; NUCIFORO, PAOLO GIOVANNI; Montuenga, Luis M ; Sánchez-Cespedes, Montse ; PRAT APARICIO, ALEIX; VIVANCOS PRELLEZO, ANA; FELIP FONT, ENRIQUETA; AMAT FERRER, RAMON. Molecular profiling of long-term responders to immune checkpoint inhibitors in advanced non-small cell lung cancer. MOLECULAR ONCOLOGY. 2021 April. 10.1002/1878-0261.12891
  • LIGERO HERNANDEZ, MARTA; Garcia-Ruiz, Alonso ; VIAPLANA DONATO, CRISTINA; VILLACAMPA JAVIERRE, GUILLERMO; Raciti, Maria V ; Landa, Jaid ; MATOS GARCIA, IGNACIO; MARTIN LIBERAL, JUAN JESUS; OCHOA DE OLZA AMAT, MARIA; HIERRO CARBO, CINTA; MATEO VALDERRAMA, JOAQUIN; Gonzalez, Macarena ; MORALES BARRERA, RAFAEL; SUAREZ RODRIGUEZ, CRISTINA; RODON AHNERT, JORDI; ELEZ FERNANDEZ, MARIA ELENA; BRAÑA GARCIA, IRENE; MUÑOZ COUSELO, EVA; OAKNIN BENZAQUEN, ANA MAZALTOB; FASANI, ROBERTA; NUCIFORO, PAOLO GIOVANNI; Gil, Debora ; RUBIO, ISABEL TERESA; SEOANE SUAREZ, JOAN; FELIP FONT, ENRIQUETA; Escobar, Manuel ; TABERNERO CATURLA, JOSEP; CARLES GALCERAN, JOAN; DIENSTMANN, RODRIGO; GARRALDA CABANAS, ELENA; PEREZ LOPEZ, RAQUEL. A CT-based Radiomics Signature Is Associated with Response to Immune Checkpoint Inhibitors in Advanced Solid Tumors. Radiology. 2021 April. 10.1148/radiol.2021200928
  • RUBIO PEREZ, CARLOTA; Planas-Rigol, Ester ; Trincado, Juan L ; BONFILL TEIXIDOR, ESTER; ARIAS PIÑEIRO, ALEXANDRA; Marchese, Domenica ; Moutinho, Catia ; SERNA ALONSO, GARAZI; Pedrosa, Leire ; IURLARO, RAFFAELLA; Martínez-Ricarte, Francisco ; ESCUDERO MONREAL, LAURA; Cordero, Esteban ; Cicuendez, Marta ; Ruiz, Sara ; Parra, Genís ; NUCIFORO, PAOLO GIOVANNI; Gonzalez, Josep ; Pineda, Estela ; Sahuquillo, Juan ; TABERNERO CATURLA, JOSEP; Heyn, Holger ; SEOANE SUAREZ, JOAN. Immune cell profiling of the cerebrospinal fluid enables the characterization of the brain metastasis microenvironment. NATURE COMMUNICATIONS. 2020 March. 10.1038/s41467-021-21789-x
  • Oliva, Marc ; MULET MARGALEF, NURIA; OCHOA DE OLZA AMAT, MARIA; Napoli, Stefania ; Mas, Joan ; Laquente, Berta ; Alemany, Laia ; Duell, Eric J ; NUCIFORO, PAOLO GIOVANNI; Moreno, Victor. INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES. Tumor-Associated Microbiome: Where Do We Stand?. 2021 February. 10.3390/ijms22031446
  • Hudecek, J. ; Voorwerk, L. ; van Seijen, M. ; Nederlof, I. ; de Maaker, M. ; van den Berg, J. ; van de Vijver, K.K. ; Sikorska, K. ; Adams, S. ; Demaria, S. ; Viale, G. ; Nielsen, T.O. ; Badve, S.S. ; Michiels, S. ; Symmans, W.F. ; Sotiriou, C. ; Rimm, D.L. ; Hewitt, S.M. ; Denkert, C. ; Loibl, S. ; Loi, S. ; Bartlett, J.M.S. ; Pruneri, G. ; Dillon, D.A. ; Cheang, M.C.U. ; Tutt, A. ; Hall, J.A. ; Kos, Z. ; Salgado, R. ; Kok, M. ; Horlings, H.M. ; Hyytiäinen, A. ; Hida, A.I. ; Thompson, A. ; Lefevre, A. ; Lazar, A.J. ; Gown, A. ; Lo, A. ; Sapino, A. ; Madabhushi, A. ; Moreira, A. ; Richardson, A. ; Vingiani, A. ; Beck, A.H. ; Bellizzi, A.M. ; Guerrero, A. ; Grigoriadis, A. ; Ehinger, A. ; Garrido-Castro, A. ; Vincent-Salomon, A. ; Laenkholm, A.-V. ; Sharma, A. ; Cimino-Mathews, A. ; Srinivasan, A. ; Acs, B. ; Singh, B. ; Calhoun, B. ; Haibe-Kans, B. ; Solomon, B. ; Thapa, B. ; Nelson, B.H. ; Gallas, B.D. ; Castaneda, C. ; Ballesteros-Merino, C. ; Criscitiello, C. ; Boeckx, C. ; Colpaert, C. ; Quinn, C. ; Chennubhotla, C.S. ; Swanton, C. ; Solinas, C. ; Hiley, C. ; Drubay, D. ; Bethmann, D. ; Moore, D.A. ; Larsimont, D. ; Sabanathan, D. ; Peeters, D. ; Zardavas, D. ; Höflmayer, D. ; Johnson, D.B. ; Thompson, E.A. ; Brogi, E. ; Perez, E. ; ElGabry, E.A. ; Stovgaard, E.S. ; Blackley, E.F. ; Roblin, E. ; Reisenbichler, E. ; Bellolio, E. ; Balslev, E. ; Chmielik, E. ; Gaire, F. ; Andre, F. ; Lu, F.-I. ; Azmoudeh-Ardalan, F. ; Rojo, F. ; Gruosso, T. ; Ciompi, F. ; Peale, F. ; Hirsch, F.R. ; Klauschen, F. ; Penault-Llorca, F. ; Acosta Haab, G. ; Farshid, G. ; van den Eynden, G. ; Curigliano, G. ; Floris, G. ; Broeckx, G. ; Gonzalez-Ericsson ; Koeppen, H. ; Haynes, H.R. ; McArthur, H. ; Joensuu, H. ; Olofsson, H. ; Lien, H.-C. ; Chen, I.-C. ; Cree, I. ; Frahm, I. ; Brcic, I. ; Chan, J. ; Ziai, J. ; Brock, J. ; Wesseling, J. ; Giltnane, J. ; Kerner, J.K. ; Thagaard, J. ; Braybrooke, J.P. ; van der Laak, J.A.W.M. ; Lemonnier, J. ; Zha, J. ; Ribeiro, J. ; Lennerz, J.K. ; Carter, J.M. ; Saltz, J. ; Hartman, J. ; Hainfellner, J. ; Quesne, J.L. ; Juco, J.W. ; Reis-Filho, J. ; Sanchez, J. ; Sparano, J. ; Cucherousset, J. ; Araya, J.C. ; Adam, J. ; Balko, J.M. ; Saeger, K. ; Siziopikou, K. ; Willard-Gallo, K. ; Weber, K. ; Pogue-Geile, K.L. ; Steele, K.E. ; Emancipator, K. ; AbdulJabbar, K. ; El Bairi, K. ; Blenman, K.R.M. ; Allison, K.H. ; Korski, K. ; Pusztai, L. ; Comerma, L. ; Buisseret, L. ; Cooper, L.A.D. ; Shi, L. ; Kooreman, L.F.S. ; Molinero, L. ; Estrada, M.V. ; Lacroix-Triki, M. ; Al Bakir, M. ; Sebastian, M.M. ; van de Vijver, M. ; Balancin, M.L. ; Dieci, M.V. ; Mathieu, M.-C. ; Rebelatto, M.C. ; Piccart, M. ; Hanna, M.G. ; Goetz, M.P. ; Preusser, M. ; Khojasteh, M. ; Sanders, M.E. ; Regan, M.M. ; Barnes, M. ; Christie, M. ; Misialek, M. ; Ignatiadis, M. ; van Bockstal, M. ; Castillo, M. ; Amgad, M. ; Harbeck, N. ; Tung, N. ; Laudus, N. ; Sirtaine, N. ; Burchardi, N. ; Ternes, N. ; Radosevic-Robin, N. ; Gluz, O. ; Grimm, O. ; NUCIFORO, PAOLO GIOVANNI; Jank, P. ; Gonzalez-Ericsson, P. ; Kirtani, P. ; Jelinic, P. ; Watson, P.H. ; Savas, P. ; Francis, P.A. ; Russell, P.A. ; Singh, R. ; Kim, R.S. ; Pierce, R.H. ; Hills, R. ; Leon-Ferre, R. ; de Wind, R. ; Shui, R. ; De Clercq, S. ; Leung, S. ; Tabbarah, S. ; Souza, S.C. ; O’Toole, S. ; Swain, S. ; Dudgeon, S. ; Willis, S. ; Ely, S. ; Kim, S.-R. ; Bedri, S. ; Irshad, S. ; Liu, S.-W. ; Goel, S. ; Hendry, S. ; Bianchi, S. ; Bragança, S. ; Paik, S. ; Wienert, S. ; Fox, S.B. ; Luen, S.J. ; Naber, S. ; Schnitt, S.J. ; Sua, L.F. ; Lakhani, S.R. ; Fineberg, S. ; Soler, T. ; Gevaert, T. ; D’Alfonso, T. ; John, T. ; Sugie, T. ; Kurkure, U. ; Bossuyt, V. ; Manem, V. ; Cámara, V.P. ; Tong, W. ; Chen, W. ; Yang, W. ; Tran, W.T. ; Wang, Y. ; Yuan, Y. ; Allory, Y. ; Husain, Z. ; Bago-Horvath, Z. Application of a risk-management framework for integration of stromal tumor-infiltrating lymphocytes in clinical trials. NPJ breast cancer. 2020 January. 10.1038/s41523-020-0155-1
  • Chic, Nuria ; Luen, Stephen J ; NUCIFORO, PAOLO GIOVANNI; Salgado, Roberto ; Fumagalli, Debora ; Hilbers, Florentine ; Wang, Yingbo ; de Azambuja, Evandro ; Làng, István ; DI COSIMO, SERENA; SAURA MANICH, CRISTINA; Huober, Jens ; PRAT APARICIO, ALEIX; Loi, Sherene. HER2-Enriched Subtype and ERBB2 Expression in HER2-Positive Breast Cancer Treated with Dual HER2 Blockade.  JNCI-JOURNAL OF THE NATIONAL CANCER INSTITUTE. 2020 January. 10.1093/jnci/djz042
  • CAPDEVILA CASTILLON, JAUME; MATOS GARCIA, IGNACIO; MANCUSO, FRANCESCO MATTIA; Iglesias, Carmela; NUCIFORO, PAOLO GIOVANNI; Zafon, Carles ; GARCIA PALMER, HECTOR; OGBAH, ZIGHEREDA; Muinos, Laura ; HERNANDO CUBERO, JORGE; Villacampa, Guillermo ; Peña, Carol E ; TABERNERO CATURLA, JOSEP; Brose, Marcia S ; Schlumberger, Martin ; VIVANCOS PRELLEZO, ANA. Identification of Expression Profiles Defining Distinct Prognostic Subsets of Radioactive-Iodine Refractory Differentiated Thyroid Cancer from the DECISION Trial. MOLECULAR CANCER THERAPEUTICS. 2020 January. 10.1158/1535-7163.MCT-19-0211
  • Cebrià-Costa, J P ; PASCUAL REGUANT, LAURA; Gonzalez-Perez, A ; Serra-Bardenys, G ; QUEROL PAÑOL, JESSICA; Cosín, M ; Verde, G ; Cigliano, R A ; Sanseverino, W ; Segura-Bayona, S ; Iturbide, A ; Andreu, D ; NUCIFORO, PAOLO GIOVANNI; Bernado-Morales, C ; RODILLA BENITO, VERONICA; ARRIBAS LOPEZ, JOAQUIN VICENTE; Yelamos, J ; de Herreros, A Garcia ; Stracker, T H ; PEIRO SALES, SANDRA. LOXL2-mediated H3K4 oxidation reduces chromatin accessibility in triple-negative breast cancer cells. 2020 January. 10.1038/s41388-019-0969-1
  • NUCIFORO, PAOLO GIOVANNI; Townend, J. ; SAURA MANICH, CRISTINA; de Azumbaja, E. ; Hilbers, F. ; Manukyants, A. ; Werutsky, G. ; Bliss, J. ; Moebus, V. ; Colleoni, M. ; Aspitia, A.M. ; Di Cosimo, S. ; Van dooren, V. ; Kroep, J. ; Ferro, A. ; Cameron, D. ; Gelber, R. ; Piccart-Gebhart, M. ; Huober, J. Nine-year survival outcome of neoadjuvant lapatinib with trastuzumab for HER2-positive breast cancer (NeoALTTO, BIG 1-06): final analysis of a multicentre, open-label, phase 3 randomised clinical trial. EUROPEAN JOURNAL OF CANCER. 2020 January. 10.1016/S0959-8049(20)30560-8
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  • Advancing a Precision Medicine Paradigm in metastatic Colorectal Cancer: Systems based patient stratification solutions (COLOSSUS, H2020).
  • OPportunity To Investigate the Microbiomes’s Impact on Science and Treatment In Colorectal Cancer (OPTIMISTICC, Grand Challenge, Cancer Research UK).
  • Desarrollo de modelos diagnósticos y pronósticos basados en la infección intratumoral por Fusobacterium y microbiota intestinal asociada en el cáncer colorectal localizado (Fundacion Mutua Madrileña, 2020-2023)
  • Development of microbiota-based diagnostic and prognostic models by mapping intratumoral Fusobacterium and associated gut microbiota in early-stage colorectal cancer (ISCIII, 2021-2024)

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