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Chapter

9

Proto-Oncogenes, Oncogenes, and
Tumor-Suppressor Genes

58

Proto-Oncogenes and Oncogenes

A. DEFINITIONS

1.

proto-oncogene is a normal gene that encodes a protein involved in stimulation
of the cell cycle. Because 
the cell cycle can be regulated at many different points,
proto-oncogenes fall into many different classes (i.e., growth factors, receptors,
signal transducers, 
and transcription factors).

2.

An oncogene is a mutated proto-oncogene that encodes for an oncoprotein in-
volved in the hyperstimulation of the cell cycle leading to oncogenesis. This is
because the mutations cause an increased activity of the oncoprotein (either a
hyperactive oncoprotein or increased amounts of normal protein), not a loss of
activity of the oncoprotein.

B. ALTERATION OF A PROTO-ONCOGENE TO AN ONCOGENE. We know now that

the vast majority of human cancers are not caused by viruses. Instead, most human
cancers are caused by the alteration of proto-oncogenes so that oncogenes are formed
producing an oncoprotein. The mechanisms by which proto-oncogenes are altered
include.

1.

Point mutation.

A point mutation (i.e., a gain-of-function mutation) of a proto-

oncogene leads to the formation of an oncogene. A single mutant allele is suffi-
cient to change the phenotype of a cell from normal to cancerous (i.e., a dominant
mutation
). This results in a hyperactive oncoprotein that hyperstimulates the cell
cycle leading to oncogenesis. Note: proto-oncogenes only require a mutation in one
allele for the cell to become oncogenic, whereas tumor-suppressor genes require a
mutation in both alleles for the cell to become oncogenic.

2.

Translocation.

A translocation results from breakage and exchange of segments

between chromosomes. This may result in the formation of an oncogene (also
called a fusion gene or chimeric gene) which encodes for an oncoprotein (also called
a fusion protein or chimeric protein). A good example is seen in chronic myeloid
leukemia (CML). CML t(9;22)(q34;q11) is caused by a reciprocal translocation
between chromosomes 9 and 22 with breakpoints at q34 and q11, respectively. The
resulting der(22) is referred to as the Philadelphia chromosome. This results in a
hyperactive oncoprotein that hyperstimulates the cell cycle leading to oncogenesis.

3.

Amplification.

Cancer cells may contain hundreds of extra copies of proto-

oncogenes. These extra copies are found as either small paired chromatin bodies
separated from the chromosomes or as insertions within normal chromosomes.
This results in increased amounts of normal protein that hyperstimulates the cell
cycle leading to oncogenesis.

I

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59

PROTO-ONCOGENES, ONCOGENES, AND TUMOR-SUPPRESSOR GENES

4.

Translocation into a transcriptionally active region.

A translocation results

from breakage and exchange of segments between chromosomes. This may result
in the formation of an oncogene by placing a gene in a transcriptionally active re-
gion. A good example is seen in Burkitt lymphoma. Burkitt lymphoma
t(8;14)(q24;q32)  
is caused by a reciprocal translocation between band q24 on
chromosome 8 and band q32 on chromosome 14. This results in placing the MYC
gene on chromosome 8q24 in close proximity to the IGH gene locus (i.e., an im-
munoglobulin gene locus) on chromosome 14q32, thereby putting the MYC gene
in a transcriptionally active area in B lymphocytes (or antibody-producing plasma
cells). This results in increased amounts of normal protein that hyperstimulates
the cell cycle leading to oncogenesis.

C. MECHANISM OF ACTION OF THE RAS GENE: A PROTO-ONCOGENE (Figure 9-1).

The diagram shows the RAS proto-oncogene and RAS oncogene action.

1.

The  RAS proto-oncogene encodes a nor-
mal G-protein with GTPase activity. The G
protein is attached to the cytoplasmic face
of the cell membrane by a lipid called far-
nesyl isoprenoidWhen a hormone binds
to its receptor, the G protein is activated.
The activated G protein binds GTP which
stimulates the cell cycle. After a brief pe-
riod, the activated G protein splits GTP
into GDP and phosphate such that the
stimulation of the cell cycle is terminated.

2.

If the RAS proto-oncogene undergoes a
mutation, it forms the RAS oncogene. The
RAS oncogene encodes an abnormal G
protein (RAS oncoprotein) where a glycine
is changed to a valine at position 12. The
RAS oncoprotein binds GTP which stimu-
lates the cell cycle. However, the RAS on-
coprotein cannot split GTP into GDP and
phosphate so that the stimulation of the
cell cycle is never terminated.

● Figure 9-1 Action of RAS Gene.

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60

CHAPTER 9

Tumor-Suppressor Genes.

tumor-suppressor gene is a normal gene that encodes a

protein involved in suppression of the cell cycle. Many human cancers are caused by loss-
of-function mutations 
of tumor-suppressor genes. Note: tumor-suppressor genes require a
mutation in both alleles for a cell to become oncogenic, whereas, proto-oncogenes only
require a mutation in one allele for a cell to become oncogenic. Tumor-suppressor genes
can be either “gatekeepers” or “caretakers.”

A. GATEKEEPER TUMOR-SUPPRESSOR GENES. These genes encode for proteins that

either regulate the transition of cells through the checkpoints (“gates”) of the cell cycle
or promote apoptosis. This prevents oncogenesis. Loss-of-function mutations in gate-
keeper tumor-suppressor genes lead to oncogenesis.

II

A LIST OF PROTO-ONCOGENES

TABLE

9-1 

Protein Encoded by

Cancer Associated with Mutations

Class

Proto-Oncogene

Gene

of the Proto-Oncogene

Growth Platelet-derived 

growth 

PDGFB

Astrocytoma, osteosarcoma

factors

factor (PDGF)

Fibroblast growth factor

FGF4

Stomach carcinoma

Receptors

Epidermal growth factor 

EGFR

Squamous cell carcinoma of lung; breast, 

receptor (EGFR)

ovarian, and stomach cancers

Receptor tyrosine kinase

RET

Multiple endocrine adenomatosis 2

Receptor tyrosine kinase

MET

Hereditary papillary renal carcinoma, 

hepatocellular carcinoma

Receptor tyrosine kinase

KIT

Gastrointestinal stromal tumors

Receptor tyrosine kinase

ERBB2

Neuroblastoma, breast cancer

Signal Tyrosine 

kinase

ABL/BCR

CML t(9;22)(q34;q11)*

transducers

Serine/threonine kinase

BRAF

Melanoma, colorectal cancer

RAS G-proteins

HRAS

Lung, colon, and pancreas cancers

KRAS
NRAS

Transcription 

Leucine zipper protein

FOS

Finkel-Biskes-Jinkins osteosarcoma

factors

Leucine zipper protein

JUN

Avian sarcoma 17

Helix-loop-helix protein

N-MYC

Neuroblastoma

Helix-loop-helix protein

L-MYC

Lung carcinoma

Helix-loop-helix protein

MYC

Burkitt lymphoma t(8;14)(q24;q32)

Retinoic acid receptor

PML/RAR

APL t(15;17)(q22;q12)

Transcription factor

FUS/ERG

AML t(16;21)(p11;q22)

Transcription factor

PBX/TCF3

Pre-B cell ALL t(1;19)(q21;p13.3)

Transcription factor

FOX04/MLL

ALL t(X;11)(q13;q23)

Transcription factor

FLI1/EWSR1

Ewing sarcoma t(11;22)(q24;q12)

PDGFB

 platelet-derived growth factor beta gene; FGF4  fibroblast growth factor 4 gene; EGFR  epidermal growth factor

receptor gene; RET

 rearranged during transfection gene; MET  met proto-oncogene (hepatocyte growth factor receptor); 

KIT

 v-kit Hardy-Zuckerman 4 feline sarcoma viral oncogene homolog; ERBB2  v-erb-b2 erythroblastic leukemia viral oncogene

homolog 2; ABL/BCR

 Abelson murine leukemia/breakpoint cluster region oncogene; BRAF  v-raf murine sarcoma viral

oncogene homolog B1; HRAS 

 Harvey rat sarcoma viral oncogene homolog; KRAS  Kirsten rat sarcoma 2 viral oncogene

homolog; NRAS

 neuroblastoma rat sarcoma viral oncogene homolog; FOS  Finkel-Binkes-Jinkins osteosarcoma; N-MYC 

neuroblastoma v-myc myelocytomatosis viral oncogene homolog; MYC

 v-myc myelocytomatosis viral oncogene homolog;

PML/RAR

  promyelocytic leukemia/retinoic acid receptor alpha; FUS/ERG  fusion (involved in t(12;16) in malignant

liposarcoma)/v-ets erythroblastosis virus E26 oncogene homolog; PBX/TCF3

 pre-B-cell leukemia homeobox/transcription factor 3

(E2A immunoglobulin enhancer binding factors E12/E47); FOX04/MLL

 forkhead box O4/myeloid/lymphoid or mixed-lineage

leukemia; FLI1/EWSR1

 Friend leukemia virus integration 1/Ewing sarcoma breakpoint region 1.

ALL 

 acute lymphoblastoid leukemia; CML  chronic myeloid leukemia; APL  acute promyelocytic leukemia; AML  acute myel-

ogenous leukemia.

D. A LIST OF PROTO-ONCOGENES (Table 9-1)

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PROTO-ONCOGENES, ONCOGENES, AND TUMOR-SUPPRESSOR GENES

B. CARETAKER TUMOR-SUPPRESSOR GENES. These genes encode for proteins that

either detect/repair DNA mutations or promote normal chromosomal disjunction dur-
ing mitosis. This prevents oncogenesis by maintaining the integrity of the genome.
Loss-of-function mutations in caretaker tumor-suppressor genes lead to oncogenesis.

C. MECHANISM OF ACTION OF THE RB1

GENE: A TUMOR-SUPPRESSOR GENE
(RETINOBLASTOMA; Figure 9-2). 
The dia-
gram shows RB1 tumor-suppressor gene action.

1.

The RB1 tumor-suppressor gene is located
on chromosome 13q14.1 and encodes for
normal RB protein that will bind to E2F
(a gene regulatory protein) such that there
will be no expression of target genes
whose gene products stimulate the cell cy-
cle. Therefore, there is suppression of the
cell cycle at the G1 checkpoint.

2.

A mutation of the RB1 tumor-suppressor
gene will encode an abnormal RB protein
that cannot bind E2F (a gene regulatory
protein) such that there will be expression
of target genes whose gene products stim-
ulate the cell cycle. Therefore, there is no
suppression of the cell cycle at the G1
checkpoint. This leads to the formation of
retinoblastoma tumor.

● Figure 9-2 Action of RB1 Gene.

3.

There are two types of retinoblastomas.
a.

In hereditary retinoblastoma (RB), the individual inherits one mutant copy
of the RB1 gene from his parents (an inherited germline mutation). A somatic
mutation of the second copy of the RB1 gene may occur later in life within
many cells of the retina leading to multiple tumors in both eyes.

b.

In nonhereditary RB, the individual does not inherit a mutant copy of the RB1
gene from his parents. Instead, two subsequent somatic mutations of both
copies of the RB1 gene may occur within one cell of the retina leading to one
tumor in one eye
. This has become known as Knudson’s two-hit hypothesis
and serves as a model for cancers involving tumor-suppressor genes.

D. MECHANISM OF ACTION OF THE TP53

GENE: A TUMOR-SUPPRESSOR GENE
(“GUARDIAN OF THE GENOME”) (Figure
9-3). 
The diagram shows TP53 tumor-sup-
pressor gene action.

1.

The  TP53 tumor-suppressor gene is lo-
cated on chromosome 17p13 and encodes
for  normal p53 protein (a zinc finger
gene regulatory protein) 
that will cause
the expression of target genes whose gene
products suppress the cell cycle at G1 by
inhibiting  Cdk-cyclin D and  Cdk-cyclin
E
. Therefore, there is suppression of the
cell cycle at the G1 checkpoint.

2.

A mutation of TP53 tumor-suppressor gene
will encode an abnormal p53 protein that
will cause no expression of target genes
whose gene products suppress the cell

● Figure 9-3 Action of TP53 Gene.

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1.

Hereditary RB is an autosomal dominant
genetic disorder caused by a mutation in
the  RB1 gene on  chromosome 13q14.1-
q14.2 
for the RB-associated protein
(p110

RB

). More than 1000 different muta-

tions of the RB1 gene have been identified,
which include missense, frameshift, and
RNA splicing mutations which result in a
premature STOP codon and a loss-of-
function mutation.

2.

RB protein binds to E2F (a gene regula-
tory protein) such that there will be no ex-
pression of target genes whose gene prod-
ucts stimulate the cell cycle at the G1
checkpoint. The RB protein belongs to the
family of tumor-suppressor genes.

3.

Hereditary RB affected individuals inherit
one mutant copy of the RB1 gene from their
parents (an inherited germline mutation)
followed by a somatic mutation of the sec-
ond copy of the RB1 gene later in life.

● Figure 9-4 Hereditary Retinoblastoma.

62

CHAPTER 9

cycle. Therefore, there is no suppression of the cell cycle at the G1 checkpoint. The
TP53 tumor-suppressor gene is the most common target for mutation in human can-
cers. The TP53 tumor-suppressor gene plays a role in Li-Fraumeni syndrome.

E.

A LIST OF TUMOR-SUPPRESSOR GENES (Table 9-2)

A LIST OF TUMOR-SUPPRESSOR GENES

TABLE

9-2 

Protein Encoded by

Cancer Associated with Mutations

Class

Tumor-Suppressor Gene

Gene

of the Tumor-Suppressor Gene

Gatekeeper

Retinoblastoma associated 

RB1

Retinoblastoma, carcinomas of the 

protein p110

RB

breast, prostate, bladder, and lung

Tumor protein 53

TP53

Li-Fraumeni syndrome; most human 

cancers

Neurofibromin protein

NF1

Neurofibromatosis type 1, Schwannoma

Adenomatous polyposis 

APC

Familial adenomatous polyposis coli, 

coli protein

carcinomas of the colon

Wilms tumor protein 2

WT2

Wilms tumor (most common renal 

malignancy of childhood)

Von Hippel-Lindau disease 

VHL

Von Hippel-Lindau disease, retinal and 

tumor-suppressor protein

cerebellar hemangioblastomas

Caretaker

Breast cancer type 1 

BRCA1

Breast and ovarian cancer

susceptibility protein

Breast cancer type 2 

BRCA2

Breast cancer in BOTH breasts

susceptibility protein

DNA mismatch repair 

MLH1

Hereditary nonpolyposis colon cancer

protein MLH1

DNA mismatch repair 

MSH2

Hereditary nonpolyposis colon cancer

protein MSH2

APC

 familial adenomatous polyposis coli; VHL  von Hippel-Lindau disease; WT  Wilms tumor; NF-1  neurofibromatosis;

BRCA

 breast cancer; RB  retinoblastoma; TP53  tumor protein; MLH1  mut L homolog 1; MSH2  mut S homolog 2.

Hereditary Cancer Syndromes

A. HEREDITARY RETINOBLASTOMA (Figure 9-4)

III

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