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 Advances in
CANCER
RESEARCH

Volume 101
This page intentionally left blank
 Advances in
CANCER
RESEARCH
Volume 101

Edited by

George F. Vande Woude

Van Andel Research Institute
Grand Rapids
Michigan, USA

George Klein
Microbiology and Tumor Biology Center
Karolinska Institute
Stockholm, Sweden

AMSTERDAM • BOSTON • HEIDELBERG • LONDON

NEW YORK • OXFORD • PARIS • SAN DIEGO
SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO
Academic Press is an imprint of Elsevier
Academic Press is an imprint of Elsevier
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First edition 2008

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ISBN: 978-0-12-374359-6
ISSN: 0065-230X

For information on all Academic Press publications

visit our Web site at www.elsevierdirect.com

Printed and bound in USA

08 09 10 11 10 9 8 7 6 5 4 3 2 1
 Contents

Contributors to Volume 101 ix

Contribution of AZAP-Type Arf GAPs to Cancer Cell

Migration and Invasion
Vi Luan Ha, Ruibai Luo, Zhongzhen Nie, and Paul A. Randazzo
I. Introduction 1
II. Signals Influenced by Arf GAPs 2
III. Cellular Adhesive Structures Affected by Arf GAPs 2
IV. The Substrates for the Arf GAPs: Arf Family GTP-Binding Proteins 5
V. The Arf GAP Family 7
VI. Arf GAP Subtypes Implicated in Carcinogenesis 10
VII. Arf GAP Subtypes that Affect Signaling or Adhesion but have not been
Implicated in Oncogenesis 18
VIII. Comparative Enzymology of the Arf GAPs 20
IX. Conclusions 21
References 21

Role and Regulation of Human Tumor Suppressor

SUFU in Hedgehog Signaling
Steven Y. Cheng and Shen Yue
I. Introduction 29
II. The Functions of Drosophila Sufu: Lessons Learned from
the Wing Imaginal Disc 31
III. The Conserved and Distinct Roles of Mammalian SUFU in Sonic
Hh Signaling 34
IV. Regulation of SUFU Activity 38
V. Sufu as a Tumor Suppressor 39
VI. Concluding Remark 39
References 40

v
vi Contents

FAK Expression: Regulation and Therapeutic Potential

Shufeng Li and Zi-Chun Hua
I. Introduction 46
II. FAK Expression and Regulation 46
III. FAK as a Tumor Therapy Target 51
IV. Perspectives 54
References 56

Adhesion Proteins Meet Receptors: A Common Theme?

Véronique Orian-Rousseau and Helmut Ponta
I. Introduction 63
II. Modulation of Signaling Receptors by CAMs 65
III. Concluding Remarks 83
References 86

The Six Family of Homeobox Genes in Development and Cancer

Kimberly L. Christensen, Aaron N. Patrick, Erica L. McCoy, and Heide L. Ford
I. Introduction 94
II. The Six Family of Homeobox Genes 96
III. The Six1 Homeobox Gene in Development and Cancer 108
IV. The Retinal Determination Network: Cofactors of the Six Family 111
V. Concluding Remarks 117
References 118

Mechanisms Regulating the Susceptibility of Hematopoietic

Malignancies to Glucocorticoid-Induced Apoptosis
Ronit Vogt Sionov, Rachel Spokoini, Shlomit Kfir-Erenfeld, Orly Cohen,
and Eitan Yefenof
I. Introduction 130
II. Mechanisms Involved in Glucocorticoid (GC)-Induced Apoptosis 132
III. Glucocorticoids and the T Cell Selection Process in the Thymus 169
IV. Glucocorticoids and Immunosuppression 173
V. Other Tissues Affected by Glucocorticoids 176
VI. Mechanisms of GC Resistance 180
VII. Overcoming Resistance to GC-Induced Apoptosis 191
VIII. Concluding Remarks 199
References 204
Contents vii

IFN Inducibility of Major Histocompatibility Antigens in Tumors

Barbara Seliger, Francisco Ruiz-Cabello, and Federico Garrido
I. The Family of Interferons and Their Function 251
II. IFN Signal Transduction Pathways and Their Components 253
III. The MHC Class I and Class II Antigen-Processing Pathways 255
IV. Defective IFN Inducibility of APM Components in Tumors 262
V. Clinical Relevance of Aberrant IFN Signaling 267
VI. Conclusions 269
References 270

The Role of NKT Cells in Tumor Immunity

Masaki Terabe and Jay A. Berzofsky
I. Introduction 278
II. Type I NKT Cells 284
III. Type II NKT Cells 301
IV. Interaction of NKT Cell Subsets With Each Other and Other Cell Types 310
V. Potential Translational Approaches 317
Conclusions 324
References 327

HIV Induced AIDS and Related Cancers: Chronic Immune

Activation and Future Therapeutic Strategies
Martin Cadogan and Angus G. Dalgleish
I. HIV/AIDS and Cancer 349
II. Brief Introduction to HIV Pathogenesis 350
III. Emergence of a Viral Triggered Immunological Disease 351
IV. Chronic Immune Activation as a Critical Component of
Pathogenic Viral Infection 352
V. Influence of Immune Activation Upon HIV 354
VI. Chronic Activation in Immune Pathogenesis, Dysfunction,
and Autoimmune Processes 356
VII. Does the HLA Repertoire Influence Susceptibility to Chronic
Immune Activation? 360
VIII. Root Causes of Chronic Immune Activation 362
IX. HLA Mimicry in AIDS Pathogenesis 365
X. Implications for Treatment and Vaccination 372
XI. Conclusion 373
References 374
viii Contents

The Cancer Cell–Leukocyte Fusion Theory of Metastasis

John M. Pawelek and Ashok K. Chakraborty
I. Introduction 398
II. Cancer Cell Fusion in vivo 401
III. Tumor-Associated Macrophages as Candidates for Cancer
Cell Fusion Partners 407
IV. Macrophage–Melanoma Fusion in vitro Generates Altered
Gene Expression and a Metastatic Phenotype in vivo 416
V. 1,6-Branched Oligosaccharides and Coarse Vesicles in
Putative Human BMT–Tumor Hybrids 423
VI. 1,6-Branched Oligosaccharides and Coarse Vesicles are
Common in Human Cancers 425
VII. Considerations for Studying Fusion in vivo 426
VII. Implications 428
References 430

Index 445
 Contributors

Numbers in parentheses indicate the pages on which the authors’ contributions begin.
Jay A. Berzofsky, Vaccine Branch, Center for Cancer Research, National
Cancer Institute, National Institutes of Health, Bethesda, Maryland, USA
(277)
Martin Cadogan, Laboratory of Oncology, Department of Cellular and
Molecular Medicine, St George’s University of London, London, United
Kingdom (349)
Ashok K. Chakraborty, Department of Dermatology and the Yale Cancer
Center, Yale University School of Medicine, New Haven, Connecticut,
USA (397)
Steven Y. Cheng, Center for Cancer Research, Nanjing Medical University,
Nanjing, Jiangsu, PR China (29)
Kimberly L. Christensen, Program in Molecular Biology, University of
Colorado School of Medicine, Denver, Colorado, USA (93)
Orly Cohen, The Lautenberg Center for General and Tumor Immunology,
The Institute of Medical Research, The Hebrew University, Hadassah
Medical School, Jerusalem, Israel (127)
Angus G. Dalgleish, Laboratory of Oncology, Department of Cellular and
Molecular Medicine, St George’s University of London, London, United
Kingdom (349)
Heide L. Ford, Department of Biochemistry and Molecular Genetics,
University of Colorado School of Medicine, Denver, Colorado and
Department of Obstetrics and Gynecology, University of Colorado School
of Medicine, Denver, Colorado, and Program in Molecular Biology,
University of Colorado School of Medicine, Denver, Colorado, USA (93)
Federico Garrido, Department of Analisis Clinicos e Inmunologia; Hospital
Universitario Virgen de las Nieves; Universidad de Granada, Granada,
Spain (249)
Vi Luan Ha, Laboratory of Cellular and Molecular Biology, National
Cancer Institute, Bethesda, Maryland, USA (1)
Zi-Chun Hua, State Key Laboratory of Pharmaceutical Biotechnology, College
of Life Science, Nanjing University, Nanjing, PR China (45)

ix
x Contributors

Shlomit Kfir-Erenfeld, The Lautenberg Center for General and Tumor

Immunology, The Institue of Medical Research, The Hebrew University,
Hadassah Medical School, Jerusalem, Israel (127)
Shufeng Li, State Key Laboratory of Pharmaceutical Biotechnology, College
of Life Science, Nanjing University, Nanjing, PR China (45)
Ruibai Luo, Laboratory of Cellular and Molecular Biology, National Cancer
Institute, Bethesda, Maryland, USA (1)
Erica L. McCoy, Program in Molecular Biology, University of Colorado
School of Medicine, Denver, Colorado, USA (93)
Zhongzhen Nie, Department of Pathology, Medical College of Georgia,
Augusta, Georgia, USA (1)
Véronique Orian-Rousseau, Institute for Toxicology and Genetics, For-
schungszentrum Karlsruhe, Karlsruhe, Germany (63)
Aaron N. Patrick, Program in Molecular Biology, University of Colorado
School of Medicine, Denver, Colorado, USA (93)
John M. Pawelek, Department of Dermatology and the Yale Cancer Center,
Yale University School of Medicine, New Haven, Connecticut, USA (397)
Helmut Ponta, Institute for Toxicology and Genetics, Forschungszentrum
Karlsruhe, Karlsruhe, Germany (63)
Paul A. Randazzo, Laboratory of Cellular and Molecular Biology, National
Cancer Institute, Bethesda, Maryland, USA (1)
Francisco Ruiz-Cabello, Department of Analisis Clinicos e Inmunologia;
Hospital Universitario Virgen de las Nieves; Universidad de Granada,
Granada, Spain (249)
Barbara Seliger, Martin Luther University Halle-Wittenberg, Institute of
Medical Immunology, Halle, Germany (249)
Ronit Vogt Sionov, The Lautenberg Center for General and Tumor
Immunology, The Institute of Medical Research, The Hebrew University,
Hadassah Medical School, Jerusalem, Israel (127)
Rachel Spokoini, The Lautenberg Center for General and Tumor
Immunology, The Institute of Medical Research, The Hebrew University,
Hadassah Medical School, Jerusalem, Israel (127)
Masaki Terabe, Vaccine Branch, Center for Cancer Research, National
Cancer Institute, National Institutes of Health, Bethesda, Maryland, USA
(277)
Eitan Yefenof, The Lautenberg Center for General and Tumor Immunology,
The Institute of Medical Research, The Hebrew University, Hadassah
Medical School, Jerusalem, Israel (127)
Shen Yue, Center for Cancer Research, Nanjing Medical University,
Nanjing, Jiangsu, PR China (29)
 Contribution of AZAP‐Type Arf
GAPs to Cancer Cell Migration
and Invasion
Vi Luan Ha,* Ruibai Luo,* Zhongzhen Nie,{ and
Paul A. Randazzo*
*Laboratory of Cellular and Molecular Biology, National Cancer Institute,
Bethesda, Maryland, USA
{
Department of Pathology, Medical College of Georgia, Augusta, Georgia, USA

I. Introduction
II. Signals Influenced by Arf GAPs
III. Cellular Adhesive Structures Affected by Arf GAPs
A. Focal Adhesions
B. Invadopodia and Podosomes
IV. The Substrates for the Arf GAPs: Arf Family GTP‐Binding Proteins
V. The Arf GAP Family
VI. Arf GAP Subtypes Implicated in Carcinogenesis
A. AGAP Proteins in Glioblastoma
B. ASAPs and Cell Invasion
VII. Arf GAP Subtypes that Affect Signaling or Adhesion But Have Not Been
Implicated in Oncogenesis
A. The ARAPs
B. ACAPs and the Regulation of Integrin
VIII. Comparative Enzymology of the Arf GAPs
IX. Conclusions
References

Arf GAPs are a family of proteins with a common catalytic domain that induces
hydrolysis of GTP bound to the small GTP‐binding protein Arf. The proteins are
otherwise structurally diverse. Several subtypes of Arf GAPs have been found to be
targets of oncogenes and to control cell proliferation and cell migration. The latter
effects are thought to be mediated by coordinating changes in actin remodeling and
membrane traffic. In this chapter, we discuss Arf GAPs that have been linked to onco-
genesis and the molecular mechanisms underlying the effects of these proteins in cancer
cells. We also discuss the enzymology of the Arf GAPs related to possible targeted
inhibition of specific subtypes of Arf GAPs. # 2008 Elsevier Inc.

I. INTRODUCTION
Carcinogenesis is a complex process involving changes in cell prolifera-
tion, apoptosis, migration, and adhesion. Signaling pathways controlling
each of these cellular activities have been identified. The mechanisms by

Advances in CANCER RESEARCH 0065-230X/08 $35.00

DOI: 10.1016/S0065-230X(08)00401-6
1
2 Vi Luan Ha et al.

which the activities are coordinated are still being discovered. Arf GAP
proteins, identified as regulators of Arf family GTP‐binding proteins, are
interfaces between signaling pathways. The Arf GAPs also function as scaf-
folds and have intrinsic activities, such as bending membranes, which may
directly contribute to the aberrant behavior of cancer cells.

II. SIGNALS INFLUENCED BY Arf GAPs

Proliferative and migration signals that are influenced by Arf GAPs are
initiated by receptor tyrosine kinases (RTKs). These are transmembrane
proteins such as epidermal growth factor receptor (EGFR) and platelet‐
derived growth factor receptor (PDGFR) (Blume‐Jensen and Hunter, 2001;
Hunter, 2000; Pawson and Scott, 1997; Schlessinger, 2000). In normal
physiology, tyrosine kinase activity in these proteins is activated by ligand
binding. At least seven polypeptide ligands, including epidermal growth
factor (EGF) and transforming growth factor (TGF ), bind to EGFR.
The peptide platelet‐derived growth factor (PDGF) binds to PDGFR. The
receptors autophosphorylate, which creates binding sites for adaptor pro-
teins and signaling proteins that contain SH2 and PTB domains. Proteins
recruited to the membrane either by direct interaction with RTKs or indi-
rectly include nonreceptor tyrosine kinases such as the oncogene Src, phos-
pholipase C , phosphatidylinositol 3‐kinase, and exchange factors for Ras
family GTP‐binding proteins and Rho family GTP‐binding proteins.
Ras
GTP stimulates the MAP kinase pathway, leading to changes in tran-
scriptional activity and, consequently, cell proliferation. Ras
GTP also sti-
mulates PI3K, which generates the signaling lipid phosphatidylinositol
3,4,5‐trisphosphate (PIP3). PIP3 activates the serine/threonine kinase Akt,
which inhibits apoptosis and stimulates protein synthesis and cell prolifera-
tion. RhoA
GTP, Rac1
GTP, and Cdc42
GTP are generated, which act
through different classes of effectors to alter the actin cytoskeleton and
change transcription leading to proliferation.

III. CELLULAR ADHESIVE STRUCTURES AFFECTED

BY Arf GAPs

Cellular adhesive structures mediate cell movement and are involved in

cellular signaling. At least three adhesive structures are affected by Arf GAPs
(Fig. 1).
Arf GAPs in Cancer 3

A
Stress fibers
Complex of proteins

Ac

Ac
Ac
forming a focal

tin

tin
tin
adhesion
Nucleus

Stress fibers
n
Vinculin
ctini
Focal adhesions Pa a-a

Talin
xil
lin
Cell membrane
a
b
ECM ECM
Integrins

ASAP3
ASAP3 Vinculin ASAP3 a-actinin

B ASAP1
Actin
Podosomes/invadopodia
Golgi Cortactin
Nucleus

Golgi

ECM ECM
ASAP1 Cortactin ASAP1 Cortactin

Fig. 1 Schematic representation of cellular adhesive structures regulated by Arf GAPs. (A)
Focal adhesions (FA). The structures are illustrated in panels using ASAP3 which colocalizes
with FA markers such as vinculin (left panels) and ‐actinin (right panels) in U118 glioblastoma
cells. (B) Invadopodia and podosomes. These structures are induced by Src activation.
To visualize invadopodia and podosomes, cells were transfected with plasmids directing the
expression of active Src. Under this condition, invadopodia and podosomes were detected using
ASAP1 and cortactin in NIH3T3 fibroblasts (left panels, arrows indicate podosomes) and
MDA‐MB‐231 breast cancer cells (right panels, arrows indicate invadopodia).
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