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. 2024 Jun;19(2):355–359. doi: 10.26574/maedica.2024.19.2.355

Clinical Impact of C-myc Oncogenic Diversity on Solid and Lymphoid Malignancies

Sotirios PAPOULIAKOS 1, Aristeidis CHRYSOVERGIS 2, Vasileios PAPANIKOLAOU 3, Despoina SPYROPOULOU 4, Georgios PAPANASTASIOU 5, Asimakis D ASIMAKOPOULOS 6, Sofianiki MASTRONIKOLI 7, Panagiotis STATHOPOULOS 8, Dimitrios ROUKAS 9, Maria ADAMOPOULOU 10, Evangelos TSIAMBAS 11, Dimitrios PESCHOS 12, Pavlos PANTOS 13, Vasileios RAGOS 14, Nicholas MASTRONIKOLIS 15, Efthymios KYRODIMOS 16
PMCID: PMC11345059  PMID: 39188831

Abstract

Introduction:

Onset and progression of malignant tumors is a multistep process including a variety of gross chromosomal and specific genes’ deregulation. Among oncogenes that are frequently altered in solid and also in hematological malignancies, the C-myc (gene locus: 8q24.21) plays a pivotal role. C-myc is a proto-oncogene encoding for a nuclear phosphoprotein implicated in cell cycle progression, apoptosis and cellular differentiation and transformation.

Objective:

The purpose of the current molecular review was to explore the differences of C-myc oncogenic activity in solid and lymphoid malignancies that modify its clinical impact on them.

Material and method:

A systematic review of the literature in the international database PubMed was carried out. The year 2010 was set as a prominent time limit for the publication date of articles in the majority of them, whereas specific references of great importance and historical value in the field of C-myc gene discovery and analysis were also included. The following keywords were used: C-myc, oncogene, signaling pathway, malignancies, carcinoma, lymphoma. A pool of 43 important articles were selected for the present study at the basis of combining molecular knowledge with new targeted therapeutic strategies.

Results:

C-myc oncogene demonstrates two different mechanisms of deregulation: amplification, mutation and translocation patterns. These particular aspects of gene alteration are unique for solid and non-solid (hematological) malignancies, respectively.

Conclusions:

C-myc is characterized by diversity regarding its deregulation mechanisms in malignancies derived from different tissues. C-myc translocation is sporadically combined with amplification (”complicon” formation) or mutations creating exotic genetic signatures. This ”bi-phasic” C-myc deregulation model in the corresponding malignant tumor categories clinically affects the corresponding patients, also modifying the targeted therapeutic strategies on them.

Keywords:C-myc, oncogene, signaling pathway, carcinoma, lymphoma.

INTRODUCTION

Gross chromosome instability (CI; polysomy/aneuploidy), speci­fic gene numerical and structural modifications (amplification, deletion, translocation point mutations) and epigenetic alterations (aberrant promoter methylation, microRNAs (MiRs) deregulation) are involved in the development and progression of solid and non-solid malignancies (1). Under the pressure of external and internal factors, normal cell microenvironment is altered, driving the cell phenotype to its neoplastic and finally malignant transformation (2). Cell cycle desynchronization, increased proliferation and decreased apoptotic death rates are crucial genetic events in this transformative procedure. Recen­tly, a new apoptosis type, called PANoptosis (PCD), has been established (3). This alternative to classical apoptosis procedure comprises different functional characteristics of apoptosis, pyroptosis and necroptosis.

Among the genes that are involved in the rise and progression of malignant tumors, over activated proto-oncogenes (oncogenes) play a key role combined with suppressor genes’ silence (4, 5). In fact, proto-oncogenes produce proteins that normally regulate cell division, proliferation and apoptosis, securing homeostasis, morphological and functional balance of the tissues (6). They are also significant components of signaling transduction pathways (7). Their deregulation gives birth to their oncogenic transformation altering the cytoplasmic and nuclear micro-environment, also implicating in the metastatic process and the epithelial-mesenchymal transition phenomenon (EMT) (8). A broad spectrum of oncogenes’ super families has been already cloned and studied in the majority of malignancies (9). In the current molecular review, we focused on the role of theC-myconcogene describing and exploring its ”bi-phasic” deregulation mechanism (amplification/translocation combined or not with mutations) in solid and non-solid (hematological) malignant tumor categories that modify the responses of the corres­ponding patients to specific targeted therapeutic strategies (Figure 1).

TheC-myconcogene/oncoprotein: structure and functions

C-myconcogene is located on chromosome 8 (gene locus: 8q24.21). The gene is a member of the family of myc proto-oncogenes that presents homology to the avian virus myelocytomatosis (V-myc) (10). In humans, this category of genes consists of three main members,C-myc,L-myc(gene locus: 1p34.2),N-myc(gene locus: 2p.24.3).C-mycencodes for a nuclear phosphoprotein that consists of 439 amino acids (62 kDa). Concerning its crystallographic structure, it is ca­tegorized as a basic helix loop-helix zipper (bHLHZip) transcription factor (11).C-mycprotein involved in normal cell cycle phase to phase G0-G1/S transition, cellular transformation, metabolism and apoptosis. At the biochemical level, theC-mycprotein product interacts with the myc-associated transcription X factor (MAX) (gene locus: 14q23.3), forming a stable heterodimer complex which binds to the E-box DNA (5’-CACGTG-3’) motif (12). This 4-helix based domain acts as a strong transcription factor regulating the expression of several target genes that regulate chromatin modification, DNA replication, mitochondrial and ribosome biogenesis. The main functions ofC-myc/MAX complex include protein binding and homo-hetero-dimeri­zation, and DNA-templated/RNA polymerase binding-transcription regulation (13). Interestingly,C-mycprotein seems to positively regulate the re-programmization of stem somatic cells, maintaining pluripotency in embryonic stem cells and acting as a member of the family of ”Yamanaka transcriptional factors” (14).

C-mycgene amplification pattern

Gene amplification is the prominent genetic mechanism that transforms proto-oncogenes into oncogenes. It is based on an abnormal production of multiple copies of a specific, restricted chromosome region. This genomic numerical abnormality called ”amplicon” is mainly detec­ted and visualized by fluorescence/chromogenic in situ hybridization (FISH/CISH) methods as isolated signals or massive, compact clusters of them (15). Amplified genes cause overexpression of the corresponding encoded proteins.C-mycamplification has been identified in a broad spectrum of solid epithelial malignancies. Concerning carcinomas derived from the digestive system,C-mycamplified cases are generally correlated with an aggressive biological behavior (increased tissue dedifferentiation, advanced stage). Many molecular studies have reported significant overexpression of the marker in colon, pharyngeal, gastric, pancreatic and hepatocellular carcinomas (16-19). Similarly, gene amplification is observed in oral and laryngeal carcinomas in low percentages, but interestingly this genetic event has been also detected in premalignant intra-epithelial lesions such as leukoplakia and dysplasia (20-23). In the field of lung carcinoma,C-mycamplification is present in low to medium percentages, but its overactivation affects multiple signaling pathways, including RAF and ERK that are essential targets for specific chemo-targeted therapy (24, 25). Additionally,C-mycamplification seems to be considered a special type of biomarker for the metastatic potential of lung carcinoma, mainly in the brain region (26, 27). Similarly, the gene is also amplified in a subset of breast carcinoma cases combined or not with specific suppressor genes’ inactivation, including retinoblastoma, but there are controversial conclusions regarding its prognostic value in the corresponding patients (28, 29). Concerning carcinomas derived from male and female reproductive organs,C-mycamplification is observed in different percentages (30).C-mycoveractivation in prostate cancer is a field of increased interest as a potential target due to its interaction with androgen/estrogen receptors (31). Interes­tingly, a very small sub set of lymphoid-type malignancies harborsC-mycgene amplifications (~2-3%) (32).

C-mycgene translocation pattern

Among all the genetic mechanisms that alter the normal cell genome, translocation is a very in­teresting paradigm of chromosomal structural rearrangement. It is the result of a re-attachment between two small chromosomal fragments. Reciprocal, non-reciprocal and robertsonian are the categories of this chromosomal structural modification (33). The most emblematic reciprocal translocation – in which two chromosomes exchange small segments with each other – involves chromosomes 2 and 9. It is called ”Philadelphia chromosome (Ph) [t(9;22) (q34:q11)]” and the result is the fusion geneBCR-ABLleading to the development of an hematological malignancy, the chronic myeloid leukemia (CML) (34).

In conjunction to the previous referred Ph translocation mechanism,C-myc/Immunoglubin heavylocus gene (IGH, gene locus: 14q32) translocation is involved in the onset and progression of lymphomas, especially in their aggressive phenotypes, such as mature B-cell lymphomas. The main type is the aggressive, relatively rare B-cell non-Hodgkin’s Epstein-Barr virus (EBV)–media­ted Burkitt lymphoma (BuL) that is characterized by the t(8;14) (q24;q32) translocation in its genetic signature (35). In BuL,C-myc/IGHtranslocation is correlated to the B cell lymphoma 6 (BCL6, gene locus: 3q27) deregulation, an anti-apoptotic, strong transcriptional process implicated in the formation of B cell germinal center, also regulating the normal proliferation and functional activity of T follicular helper cells (36). Although this specific translocation is the main mechanism in BuL, sporadic cases harborC-mycmutations, combined or not with other genes, such asTP53,CCND3,IDE3, andTCF3(37). In contrast to BuL,C-myc/BCL2-BCL6translocation are frequently detected in diffuse large B-cell lymphoma (DLBCL) involving alsoBCL1A,ICAR0S49,PAX5gene rearrangements (38). In these lymphoid malignancies, the ”complicon” phenomenon has been reported based on the translocated allele that it is also amplified, whereasC-mycpure gene amplification is observed in a very small fragment of them (39). Additionally,C-myctranslocations are identified in very aggressive lymphomas including plasmablastic (PBL) and in intermediate/unclassified B cell lymphomas, whereas noC-myctranslocation has been reported in analyzed anaplastic lymphoma kinase (ALK)- positive LBLCs, although its oncogenic activity is obviously due to its protein overexpression mediated in a few sporadic cases by amplification (40-42). It seems that, in these LBLCs, the main mechanism ofC-mycgene activation is mediated by STAT3 phosphorylation that is motivated by ALK protein (43).

In conclusion,C-mycis a critical proto-oncogene for the malignant tumor genesis process, which is transformed into an oncogene by a va­riety of mechanisms, including amplification, translocation and point mutations. Gene amplification is the prominent pattern in solid malignancies, whereasC-myc/IGH t(8;14) (q24; q32) translocation, combined or not with sporadic mutations and amplifications, affects the onset and progression of aggressive LBLC histo-types.C-mycis characterized by diversity regarding its deregulation mechanisms in malignancies derived from tissues characterized by differences in their embryonic origin (epithelial/mesenchymal). Additionally,C-myctranslocation is combined with amplification (”complicon” formation) or mutations creating exotic genetic signatures in sporadic aggressive lymphoma cases, which is a crucial observation for handling oncological patients based on their specific molecular substrate.q

Authors’ contributions: conception and design: ET and SP; drafting of the article: ET, AC, VP, DR, PS, PP, SF, GP and MA; critical revision for important intellectual content: SD, SD, EK, DP; approval of the final version of the manuscript: VR, EK, NM.

Conflicts of interest: none declared.

Financial support: none declared.

FIGURE 1.

FIGURE 1.

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Ideogram of C-myc gene different deregulation mechanisms in malignancies of epithelial and lymphoid origin. a)C-myc/IGHtranslocation; b)C-mycamplification; c)C-mycpoint mutation; d) AmplifiedC-myc/IGHtranslocation (complicon formation). In epithelial malignancies (carcinomas), gene amplification and mutations are the leading patterns ofC-myconcogenic transformation, whereas in aggressive lymphomas translocation with sporadic amplification (complicon) /mutations is the prominent mechanism.

Contributor Information

Sotirios PAPOULIAKOS, Department of Otolaryngology,‘’Gennimatas’’ GNA Hospital, Athens, Greece.

Aristeidis CHRYSOVERGIS, Department of Otolaryngology, ‘’ELPIS’’ GNA Hospital, Athens, Greece.

Vasileios PAPANIKOLAOU, Department of Otolaryngology, ‘’Sotiria’’ GNA Hospital, Athens, Greece.

Despoina SPYROPOULOU, Department of Radiation Oncology, Medical School, University of Patras, Patras, Greece.

Georgios PAPANASTASIOU, Department of Otorhinolaryngology, Head and Neck Surgery, Lausanne University Hospital, Lausanne, Switzerland; Department of Maxillofacial Surgery, Medical School, University of Ioannina, Ioannina, Greece.

Asimakis D. ASIMAKOPOULOS, Department of Otorhinolaryngology, Head and Neck Surgery, Lausanne University Hospital, Lausanne, Switzerland; Department of Maxillofacial Surgery, Medical School, University of Ioannina, Ioannina, Greece

Sofianiki MASTRONIKOLI, Brighton and Sussex Medical School, Brighton, UK.

Panagiotis STATHOPOULOS, Department of Maxillofacial Surgery, ”KAT”, GNA Hospital, Athens, Greece.

Dimitrios ROUKAS, Department of Psychiatry, 417 Veterans Army Hospital, Athens, Greece.

Maria ADAMOPOULOU, Biomedical Sciences Program, Department of Science and Mathematics, Deree American College, Athens, Greece.

Evangelos TSIAMBAS, Department of Cytology, 417 Veterans Army Hospital, Athens, Greece.

Dimitrios PESCHOS, Department of Physiology, Medical School, University of Ioannina, Greece.

Pavlos PANTOS, First Department of Otolaryngology, ”Hippocration” Hospital, Medical school, National and Kapodistrian University of Athens, Athens, Greece.

Vasileios RAGOS, Department of Otorhinolaryngology, Head and Neck Surgery, Lausanne University Hospital, Lausanne, Switzerland; Department of Maxillofacial Surgery, Medical School, University of Ioannina, Ioannina, Greece.

Nicholas MASTRONIKOLIS, Department of Otolaryngology, Medical School, University of Patras, Greece.

Efthymios KYRODIMOS, First Department of Otolaryngology, ”Hippocration” Hospital, Medical school, National and Kapodistrian University of Athens, Athens, Greece.

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