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Cell Fusions pp 351–394Cite as

Cancer Cell Fusion with Myeloid Cells: Implications for Energy Metabolism in Malignant Hybrids

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Abstract

It is abundantly clear that metastasis – the migration of cancer cells from their site of origin to distant organs and tissues – is what makes cancer so deadly. It is therefore surprising that so little is known about its onset. We advocate that the century-old theory of cancer cell fusion with tumor-associated leucocytes such as macrophages is the only complete theory we have – potentially explaining most if not all aspects of metastasis, most notably its initiation. The fusion theory states that acquisition of a metastatic phenotype occurs when a healthy migratory leucocyte fuses with a primary tumor cell. The resultant hybrid adapts the white blood cell natural ability to migrate around the body, all the while continuing to go through the uncontrolled cell division of the original cancer cell. Here we review the evidence supporting these concepts. We further focus on autophagy, a common state of macrophages that is also a signature trait of experimental macrophage-melanoma hybrids in culture. We found autophagy to be widespread in pathology specimens of human malignant melanomas, suggesting that autophagy provides an alternate energy source to these tumors. It is proposed that autophagy in melanoma and other malignancies might be a reflection of fusion with myeloid cells. Thus pathways regulating autophagy as well as the fusion events themselves provide potential new targets for cancer therapy.

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Abbreviations

ABC:

ATP-binding cassette

ALM:

Acral lentigenous melanoma

BMDC:

Bone marrow-derived cell

CCL2:

Chemokine (C-C motif) ligand 2

c-Met:

The cognate receptor for HGF

CSF:

Colony stimulating factor

CXCR4:

Cysteine-X-cysteine chemokine receptor 4

DEJ:

Dermal epidermal junction

EM:

Electron microscopy

EMT:

Epithelial-mesenchymal transition

FISH:

Fluorescent in situ hybridization

GnT-V:

N-acetylglucosaminyltransferase V

H&E:

Hematoxylin and eosin

HGF:

Hepatocyte growth factor

HIF-1:

Hypoxia-inducible factor 1

IL:

Interleukin

LAMP:

Lysosome associated membrane protein

LC3B:

Light chain 3 isoform B (autophagy marker)

LPHA:

Leucocytic phytohemagglutinin,

MC1:

Melanocortin-1

MC1R:

Melanocortin-1 receptor

M-CSF:

Macrophage-colony stimulating factor

MDR:

Multi-drug resistance

MIS:

Melanoma in situ

MITF:

Microphthalmia-associated transcription factor

PCC:

Premature chromosome condensation

PEG:

Polyethylene glycol

prcc:

Primary papillary rcc

Rcc:

Renal cell carcinoma

sialyl lex:

Sialyl lewisx antigen

SPARC:

Secreted protein acidic and rich in cysteine; osteonectin; BM40

SSM:

Superficial spreading melanoma

TAM:

Tumor associated macrophages

TGF-β1:

Transforming growth factor-β1

TR:

Toll receptor

uPA:

Urokinase-type plasminogen activator

uPAR:

uPA receptor

VEGF:

Vascular endothelial growth factor

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Acknowledgments

We gratefully acknowledge the many and invaluable contributions of David Bermudes, Jean Bolognia, Douglas Brash, Dennis Cooper, Lynn Margulis, Josh Pawelek, James Platt, Michael Rachkovsky, Stefano Sodi, and Yesim Yilmaz. Supported in part by a gift from Amway, Inc.

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  1. Department of Dermatology, Yale Cancer Center, Yale University School of Medicine, New Haven, CT, 06520-8059, USA

    Rossitza Lazova, Ashok K. Chakraborty & John M. Pawelek

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  1. Rossitza Lazova
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  1. Faculty of Life Sciences, Division of Cell Biology, University of Copenhagen, Gronnegaardsvej 7, Frederiksberg C, 1870, Denmark

    Lars-Inge Larsson

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Lazova, R., Chakraborty, A.K., Pawelek, J.M. (2011). Cancer Cell Fusion with Myeloid Cells: Implications for Energy Metabolism in Malignant Hybrids. In: Larsson, LI. (eds) Cell Fusions. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9772-9_16

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