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| Regulatory signaling network in the tumor microenvironment of prostate cancer bone and visceral organ metastases and the development of novel therapeutics |
Gina Chia-Yi Chua,Leland W.K. Chunga,*( ),Murali Gururajana,b,Chia-Ling Hsiehc,Sajni Jossona,d,Srinivas Nandanaa,e,Shian-Ying Sungc,Ruoxiang Wanga,Jason Boyang Wua,f,Haiyen E. Zhaua
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a Uro-Oncology Research, Department of Medicine and Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA
b Bristol-Myer Squibb Company, Princeton, NJ, USA
c Department of Urology, Emory University School of Medicine, Atlanta, GA, USA
d Oncoveda Cancer Research Center, Genesis Biotechnology Group, Hamilton, NJ, USA
e Texas Tech University Health Sciences Center, Department of Cell Biology and Biochemistry, Lubbock, TX, USA
f Department of Pharmaceutical Sciences, College of Pharmacy and Pharmaceutical Sciences, Washington State University, Spokane, WA, USA |
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Abstract This article describes cell signaling network of metastatic prostate cancer (PCa) to bone and visceral organs in the context of tumor microenvironment and for the development of novel therapeutics. The article focuses on our recent progress in the understanding of: 1) The plasticity and dynamics of tumor-stroma interaction; 2) The significance of epigenetic reprogramming in conferring cancer growth, invasion and metastasis; 3) New insights on altered junctional communication affecting PCa bone and brain metastases; 4) Novel strategies to overcome therapeutic resistance to hormonal antagonists and chemotherapy; 5) Genetic-based therapy to co-target tumor and bone stroma; 6) PCa-bone-immune cell interaction and TBX2-WNTprotein signaling in bone metastasis; 7) The roles of monoamine oxidase and reactive oxygen species in PCa growth and bone metastasis; and 8) Characterization of imprinting cluster of microRNA, in tumor-stroma interaction. This article provides new approaches and insights of PCa metastases with emphasis on basic science and potential for clinical translation. This article referenced the details of the various approaches and discoveries described herein in peer-reviewed publications. We dedicate this article in our fond memory of Dr. Donald S. Coffey who taught us the spirit of sharing and the importance of focusing basic science discoveries toward translational medicine.
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Received: 01 September 2018
Available online: 28 November 2018
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Corresponding Authors:
Leland W.K. Chung
E-mail: leland.chung@cshs.org
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Schematic diagram illustrates the concept of tumor cell recruitment and reprogramming in the tumor microenvironment. Through cell-cell interaction, MIC in the tumor microenvironment has the potential of recruiting resident bystander cells or indolent or dormant PCa cells, resulting in reprogramming these cells to express increased EMT, stemness, and NE phenotypes through RANK and c-Met-mediated activation of FOXM1-c-Myc/Max-AP4 signaling to promote PCa progression and metastases. Results of these series of studies emphasize the importance of tumor microenvironment driving cancer progression and metastasis through epigenetic reprogramming. EMT, epithelial to mesenchymal transition; NE, neuroendocrine; PCa, prostate cancer; RANK, the receptor activator of NF-κB; MIC, metastasis-initiating cells; RANKL, receptor activator of NF-kB ligand; AR, androgen receptor..
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Gene-based therapies for mCRPC demonstrated in our studies by dually targeting tumor-stromal interactions in multiple steps of the metastatic cascade. Therapeutic targets in primary and metastatic sites against both PCa and cancer-associated stromal cells are outlined. This figure summarizes our concept of therapeutic co-targeting of tumor and stroma using gene therapeutic approaches. This concept is based on our observation that PCa cells, upon progression to develop bone metastatic potential, expressed high levels of genes mimicking the bone, or exhibiting osteomimicry phenotype, such as expressing non-collagenous bone-like proteins, osteocalcin (OC), osteopontin (OPN), osteonectin (ON) and bone sialoprotein (BSP). We constructed both replication-deficient and -competent adenoviral vectors using the bone-like protein promoters driving either therapeutic gene, thymidine kinease (TK), or E1, that render the viruses to become replication competent, to co-target both tumor and bone compartments, and observed cytotoxic effects against tumor growth in mouse skeleton. We have also observed beneficial effects in PCa tumor regression in mice at various anatomical sites by targeting cell-matrice interactions. We observed ECM-integrin interaction via αvβ3 and αvβ5, or interaction of PCa-cell adhesion-intermediate filament complex, through L1 cell adhesion molecule (L1CAM), can be effectively targeted by target-specific siRNA constructs. EMT, epithelial to mesenchymal transition; MET, mesenchymal to epithelial transition; mCRPC, metastatic castration-resistant prostate cancer; PCa, prostate cancer; ECM, extracellular matrix.
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Factors modulating co-evolution of PCa and cancer-associated stromal cells. Diagram depicting the interaction of factors in the prostate primary tumors (seed) and the bone metastatic site (soil) with components of the immune microenvironment during the progression of the metastatic PCa. We identified additional molecular targets that can be manipulated in PCa local tumor growth and PCa tumor growth in bone. This includes inhibition of CXCR4 receptor and Wnt 3a in the primary PCa, and CXCL12 and RANKL-RANK communication in bone metastatic PCa. RANKL, receptor activator of NF-κB ligand; RANK, receptor activator of NF-κB; PCa, prostate cancer; CXCR4, CXC chemokine receptor 4; MMP-9, metalloproteinases-9; MMP-2, metalloproteinases-2.
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