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Fluorescence Guided Activatable Cancer Theranostics: Its Development and Prospect
DOI: http://ITexLi.115104
Site-specific and far-red-light-activatable
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prodrug of combretastatin A-4 using
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bc500376j
[70] Karthik S, Kumar BP,
Gangopadhyay M, Mandal M, Singh NP.
A targeted, image-guided and dually
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[71] Toupin NP, Arora K, Shrestha P,
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B flip the light switch on cancer cell
apoptosis. ACS Chemical Biology.
2019;(12):2833-2840. DOI:10.1021/
acschembio.9b00711
theranostic prodrug system activated
by reactive oxygen species for regional
chemotherapy of metastatic cancer.
Angewandte Chemie International
Edition. 2022;:e202116807.
DOI:10.1002/anie.202116807
[75] Mehlen P, Puisieux A. Metastasis: A
question of life or death. Nature Reviews
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[76] Sunwoo K, Won M, Ko KP,
Choi M, Arambula JF, Chi SG, et al.
Mitochondrial relocation of a common
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approach to cancer therapy. Chem.
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chempr.2020.03.004
[77] Xiong J, Wang P, Son S, Zhong C,
Zhang F, Mao Z, et al. Engineering a
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matt.2022.02.019
[72] Jangili P, Kong N, Kim JH, Zhou J,
Liu H, Zhang X, et al. DNA-damageresponse-targeting mitochondriaactivated multifunctional prodrug
strategy for self-defensive tumor therapy.
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DOI:/10.1002/anie.202117075
[73] Sharma A, Lee MG, Shi H,
Won M, Arambula JF, Sessler JL, et al.
Overcoming drug resistance by targeting
cancer bioenergetics with an activatable
prodrug. Chem. 2018;(10):2370-2383.
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[74] Liu L, Liu F,Liu D,Yuan W,
Zhang M, Wei P, et al. A smart
Chapter 4
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Cancer Theranostics:
Pharmaceutical View
GayathriRajaram, AlagumuruganAlagaraswamy,
MuthukumarSubramanian and VineshaRavi
Abstract
Cancer is undeniably a scary disease that leads to morbidity and mortality. With
the state-of-the-art advances, chemotherapy has made incredible strides, but the efficiency is still questionable. Diagnosing and treating cancer are necessary to effectively
approach the disease. Theranostics is a hybrid technique that combines therapeutics
and diagnostics. The key to cancer therapy is targeted drug delivery, which specifically kills cancer cells without harming healthy cells. The idea of targeted therapy is
merely a theoretical expectation that the drug will reach the target site. As seeing is
believing, theranostics helps visualize the drug delivery with the combination of diagnostic agents. Clinical settings have extensively examined the field of theranostics.
This chapter goes into great length about the potential targets and radioisotopes in
theranostics.
Keywords: theranostics, cancer, chemotherapy, targeted drug delivery,
nano-theranostics
. Introduction
Cancer is an intractable condition that has remaining a challenge for patients and
physicians for several decades. Cancer is a complex disease that is one of the leading
causes of morbidity and mortality worldwide. It is caused due to abnormal behavior
of the cells that divide in an unusual manner [1]. According to the World Health
Organization, alcohol consumption, tobacco use, diet, chemical exposure, and pollution are the major risk factors for cancer [2]. For the year 2023, the American Cancer
Society has anticipated 1,958,310 new cancer cases with a shocking 609,820 deaths
associated with cancer [3]. Cancer is conventionally treated by surgery, radiation
therapy, chemotherapy, hormonal therapy, and immunotherapy [4, 5]. Despite of the
modern advancements, cancer is still a nightmare. Targeting a cancer cell with high
specificity is required as the cancer stem cells are responsible for tumor propagation
[6]. The resistance developed by the body against the anticancer agents is also considered. Conventional chemotherapeutic agents are generally toxic and less specific in
nature. One major noticeable cause is the delay and difficulties in cancer diagnostics.
Cancers of the esophagus and pancreas are silent killers as they do not show any early
signs for detection [7]. Some recent advances in cancer diagnosis are listed in Table .
Smart Drug Delivery Systems – Futuristic Window in Cancer Therapy
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S. No Technique Description
1. Molecular imprinting Positron emission tomography (PET), computed tomography (CT)
2. Microfluidics Imaging via 2D and 3D cell culture
3. Immunosenors Affinity-based biosensors
4. Optoelectric systems Use of light emission
5. Theranostics Therapeutics + diagnosis
Table 1.
Cancer diagnostic techniques.
Theranostics is a combinatory term that combines therapeutics and diagnostics.
Theranostic approach enables targeted, quick, and effective treatment, minimizing
multi-step procedures in diagnosis and treatment. It is an easier system that allows the
switch from diagnostic to therapeutic agent. It is a personalized drug delivery system
that can be modified based on the requirements of the patients [8]. For this purpose,
radioactive agents and radiotherapeutic approach are used [9].
. Potential targets in cancer theranostics
In order to serve as both diagnostic and therapeutic approaches, theranostic agent
is made up of biomarkers with radioactive material. The radioactive nature of the
system enables visualization through molecular imaging techniques like Positron
Emission tomography (PET), Computerized tomography (CT), and single-photon
S. NO Condition Ta rge t Example of theranostic agent Reference
1. Thyroid
cancer
2. Neuroendocrine
cancer
3. Pancreatic
cancer
4. Prostate
cancer
5. Breast
cancer
6. Ovarian
cancer
Sodium iodine symporter,
glucose transporter, amino
acid transporter and
nucleoside transporter
Neuroendocrine cells meta-iodobenzylguanidine
CA19.9 (cancer antigen
19.9), MUC1 (glycoprotein
mucin 1), and TAG72
(tumor associated
glycoprotein 72
Prostate-specific
membrane antigen
HER2 [89Zr] Zr-trastuzumab
Cancer antigen CA125
Radioactive iodine 131[131I]
18
[
F]tetrafluoroborate ([18F]
TFB)
18
[
F]fluoroglutamine ([18F]
FGln)
(MIBG)
68
Ga, 99mTc, and 123/124/131-I [19]
177lutetium-[DOTA°,Tyr3]
octreotate (177Lu-DOTATATE)
195
Pt-cisplatinum
89Zr-trastuzumab
Table 2.
Cancer theranostic targets.
[11–14]
[15–17]
[18]
[20–22]
[23, 24]
Cancer Theranostics: Pharmaceutical View
DOI: http://ITexLi.113913
emission computed tomography (SPECT) [10]. The theranostic targets of common
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cancers are summarized in Table
.
. Thyroid-cancer
Theranostics hold enormous potential in the treatment of cancer. Thyroid can
cer is an endocrine malignancy observed among 1% of new cases each year [25].
Radioiodine therapy is a well-established technique used for treating thyroid cancer
in post-surgical cases [26]. Radioactive Iodine 131[
131
I] is the oldest theranostic
agent, still being widely used. Uptake of radioactive iodine is promoted by high
levels of Thyroid Stimulating Hormone (TSH) [11]. Apart from radioactive iodine
[18F] fluoro-D-glucose ([18F] FDG) is another widely used theranostic marker. The
theranostic agents target cellular transporters like sodium iodine symporter (NIS),
glucose transporter (GT), amino acid transporter (AAT), and nucleoside transporter
(NT). NIS facilitates the movement of sodium and iodide ions in and out through
the cell membrane. Agents like [
131
I] and [18F] tetrafluoroborate ([18F] TFB) have a
high affinity towards NIS and get transported into the thyroid cancer cells where
overexpression can be noticed [12]. Figure
131
Iodine and [18F] Tetrafluoroborate tracers. [18F] fluoro-D-glucose [18F] FDG, being
shows the comparative visualization of
a glucose analog, is transported through GT and visualized by PET scan [13]. In some
cases, [18F] FDG yields false positive results, to address that alternate AAT targeting
agents like L-[methyl-11C]-methionine ([11C] MET), and [18F] fluor glutamine ([18F]
FL) are gaining attention [14]. It is also noticeable that NT targeting agents are still
being studied and remain in the development stage.
. Neuro-endocrine cancer
Iodine-131-meta-iodobenzylguanidine is a form of radiotherapy that contains
meta-iodobenzylguanidine (MIBG) with trace amounts of radioactive iodine. MIBG
is a guanidine derivative used for imaging and therapy of neuroendocrine tumors and
Figure 1.
Comparison of
131
Iodine and [18F] Tetrafluoroborate tracers [13].
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neuroblastoma [15, 27]. Neuroblastoma is pictured by extracranial tumors. MIBG is the
preferred diagnostic agent as it exhibits high specificity and selectivity [28]. 123I-MIBG
and 131I-MIBG are used in clinical imaging studies, more effective in stage IV neuroblastoma as they offer better visibility [29]. As the I-MIBG structurally resembles norepinephrine, it is easily taken up by the neuroendocrine cells [16, 17]. However, it must be brought
to attention that acute thyroid blockade is necessary before I-MIBG use, as the iodine
complex is most likely absorbed by the thyroid glands [30]. 18F-fluorodeoxyglucose-based
PET/CT scans are employed in the case of early-stage neuroblastoma [31].
. Pancreatic cancer
Pancreatic cancer is the deadliest form of cancer. Pancreatic cancer is usually
asymptomatic or exhibits minimal symptoms, making it difficult to diagnose in its
initial stages. Theranostics is a sensible approach for efficient diagnosis and treatment
of cancer that has a very low survival rate [32]. CA19.9 (cancer antigen 19.9), MUC1
(glycoprotein mucin 1), and TAG72 (tumor-associated glycoprotein 72) have been the
major targets for pancreatic cancer theranostics [18, 23].
. Prostate cancer
Cancer of the prostate is the second most common type of cancer occurring
in men. The etiology of prostate cancer is less known compared to other types of
cancers. The risk factors include age, lifestyle, diet, chemical exposure, obesity, infection, and more [33, 34]. The first line treatment of prostate cancer is targeting the 5-α
reductase enzyme. The 5-α reductase is responsible for conversion of testosterone to
dihydrotestosterone, which promotes prostate cancer. 5-α reductase inhibitors like
finasteride are effective chemo-preventive agents [35, 36]. Along with this, androgendepriving agents and chemotherapy can be employed. In recent years, hormonal
agents, namely abiraterone and enzalutamide, depicted better results [37].
Prostate-specific membrane antigen (PSMA), also known as glutamate carboxypeptidase II, is a membrane-bound glycoprotein that is normally found in healthy
prostate cells but is present in abnormally high concentrations in prostate cancer [38].
PSMA imaging acts as a vital diagnostic tool in prostate cancer. PSMA radioligand
therapy (PRLT) is a technique where ligands associated with PSMA are combined
with a radioactive isotope to serve as a theranostic agent [39]. In recent years, PSMA
has been visualized using radioactive nuclei like
68
Ga radiopharmaceutical is the first FDA-approved gallium system for PET imaging
68
Ga, 99mTc, and 123/124/131-I.
prostate cancer in 2020. PSMA 11 is of major focus in prostate cancer.
[68Ga]Ga-PSMA-11 is widely used for initial diagnosis, prostate cancer staging,
and metastases. It is formed by complexation of Ga with hexadentate chelator with
octahedral geometry. It has relatively short half-life of about 67.6minutes. Now [68Ga]
Ga-PSMA-11 is available as ready-to-use injectable solution [19].
Hofman et al., studied and reported that the [68Ga] Ga-PSMA-11 has excellent
specificity and selectivity compared to conventional imaging techniques [40].
Bombesin is a prostate cancer growth factor, overexpressed in malignancy. Bombesin
is coupled with technetium-99m which serves as a theranostic agent to detect and
stage prostate cancer. Scopinaro
et al., mentioned that the use of
99m
TC-Bombesin is
sufficiently high for diagnosing prostate cancer [41]. Morris et al., combined anticancer agent docetaxel with radium-223 which was well tolerated and might have efficacy
compared to docetaxel alone [42, 43].
Cancer Theranostics: Pharmaceutical View
DOI: http://ITexLi.113913
. Breast cancer
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Breast cancer is a deadly form of cancer that concerns the women population. The
happy relief is that about 80% of the breast cancer is curable [44]. Breast biopsy is
the ultimate method of diagnosing breast cancer, however, imaging studies such as
mammography and MRI are prominent tools [45].
The oncogene of breast cancer, HER2 (human epidermal growth factor receptor 2)
can be targeted through trastuzumab radiolabeled with Indium-111, Cu-trastuzumab,
and [89Zr] Zr-trastuzumab. Coupling monoclonal antibodies such as trastuzumab
with 177Lu and bifunctional chelating agents enables HER2 targeting. Lu is a gamma
emitter which comes with minimal toxicity [20, 21]. 177Lutetium- [DOTA°, Tyr3]
octreotate (177Lu-DOTATATE) is an FDA-approved radionucleotide therapy,
recommended for gastropancreatic neuroendocrine tumors [22]. Fibroblast activation protein (FAP) is expressed in cancer-associated fibroblasts. FAP inhibitors are
preferred for their diagnostic and therapeutic value [46]. Jokar et
al., reported that
five patients who demonstrated relapse under conventional therapy responded well
with 177Lu-trastuzumab (Herceptin), 177Lu-DOTATATE, and 177Lu-FAPI-46 [47].
To develop a robust diagnostic tool, theranostics revolves around specific targets.
One of the recent advancements is using radioactive ligands to target human epidermal growth factor receptor 2 (HER-2) in breast cancer [48]. Anti-HER2 therapy
is widely used in the treatment of breast cancer [49]. Trastuzumab is an anti-HER2
monoclonal antibody. Trastuzumab is coupled with radioactive isotope to promote a
highly specific diagnostic aid [50]. Indium-111 with trastuzumab is used in SPECT
with remarkable results [51].
Copper-64 is another positron-emitting radionuclide that has a preferable half-
life, making it a vital diagnostic agent, compared to other radioactive isotopes [52].
Carrasquillo et
al
., studied the use of [64Cu] Cu-trastuzumab in detecting breast
cancer and its brain metastasis and concluded that it is safe, practical, and effective
[52]. Zirconium is a radioactive metal with the longest half-life [52]. Dijkers et
al
.,
brought to interesting notice that [89Zr] Zr-trastuzumab was sufficient to assess the
tumors even after 4–5days post single-dose injection. However, it is dose dependent
and accumulation was observed to increase with time [53].
Beylergil
al
et
., used F(ab′), a fragment of immunoglobulin G, with 1,4,7,10-tet-
raazacyclododecane-N, N′, N′′, N′′′-tetra acetic acid (DOTA) and trastuzumab and
68
68
synthesized DOTA-F(ab′)2-trastuzumab. It is further radiolabelled with
Ga.
Ga
DOTA-F(ab′)2-trastuzumab and reported that the reagent was safe with favorable
pharmacokinetics [54].
Guo
imaging. It is evident that
in diagnosis of HER2-positive cancer [55]. Bhusari et
et al., developed an Iodine-124 coupled trastuzumab for noninvasive PET
124
I-Trastuzumab had high tumor uptake and can be used
., used
al
177
Lu-trastuzumab to
target HER-2 and described its active intake in HER-2 positive breast cancer [56].
. Ovarian cancer
Cancer of the ovaries is one of the lethal forms of cancer. Despite its invasiveness,
due to a lack of suitable biomarkers, it goes undiagnosed in early stages. Delayed
diagnosis leads to impaired treatment. Near-infrared photoimmunotherapy is a theranostic approach in which a conjugate of antibody and photo absorber. This targets
the cancer cells and enables visualization with the support of infrared light [57].
Recurrent ovarian cancer is resistant to traditional therapy. 89Zr-DFO-mAb-B43.13,
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89Zr-trastuzumab, and PLGA-RbCur-gadolinium complex are some examples of
theranostic agents used to target, folate receptors, CA125, and HER2 involved in ovarian cancers [58].
CA125 is a cancer antigen over-expressed in ovarian cancer. It acts as a remarkable target cell in cancer theranostics. Antibodies specific to CA125 are used in PET
imaging [23]. Zirconium is coupled with an anti-CA125 antibody and evaluated in
animal models by Sharma et al. [59]
theranostics.
Zeevaart et al., produced
emphasized that
195
Pt-Cisplatinum could serve as a highly specific diagnostic tool
195
99m
Tc is also widely explored in ovarian cancer
Pt-Cisplatinum as a part of phase 0 clinical trial. They
with good specificity [24]. Astatine is an alpha emitter used in diagnostics. Hallqvist
et al., formed 211At-monoclonal murine antibody complex to target and treat small
tumors. The agent was administered as an intraperitoneal injection to patients who
exhibited only low-grade toxicity [60].
. Radioactives in theranostics
Radionuclides are the heart of theranostics. To enable visualization, radioisotopes are necessary. Radionuclides can be identified as alpha, beta, or gamma
emitters. Alpha emitters usually transfer high energy to the target tumor with a
short range of 50–100μm, so that it does not affect the surrounding cells [61].
Radium-223 (223Ra) decay and thorium-227 (227Th) are the commonly used
alpha emitters [62].
Beta emitters are found to have high energy that ends up damaging the DNA and
causing cell death [63]. The most commonly used radionuclides are gamma emitters.
Gamma emitters produce good-quality imaging via planar imaging or SPECT [60].
The most seen radioisotopes are 123,124I/131I, 99mTc, 43,44Sc/46,47Sc,60,61,64Cu,
68Ga, 177Lu, and 197Au/198Au in some cases [64].
Copper is available in four isotopic forms 67Cu, 64Cu, 61Cu, and 60Cu. Copper is
a metal present in micro quantity in human body. It is learned that accumulation of
copper is more common in malignant tissues than in normal tissues. This favors the
tumor-targeted approach [65, 66]. Copper-based theranostic agents are more specific, pure, and easy to produce.
Gallium, mainly 68Ga, has a long-standing history in theranostics. It is a beta emitter more frequently used in cancer theranostics, involving various organs. 68Ga has
half-life of 68.1minutes. Gallium is also used in combination with chelating agents.
68
Ga-DOTATATE injection NETSPOT was approved by USFDA in 2016 for imaging
neuroendocrine tumors [67, 68].
Radioactive iodine is ideally one of the first radionuclides used in theranostics.
131
I is used in diagnosing thyroid diseases.
thyroid cancer. Therapeutically
131
I is also used in tumor hypoxia [69].
Lutetium-177 is a gamma emitter that is desirable in cancer theranostics. It can
emit both particulate and electromagnetic radiation, which enables spontaneous
imaging and treatment [70].
All the theranostic agents require a visualizing aid to the provide diagnosis. The
success of every theranostic agent lies in the apt diagnostic aid. PET is one such
technique that is enormously used in cancer diagnosis. Since the ninteenth century,
several hybrid visualization techniques such as SPECT-PET have been extensively
used [71]. The tracers are exclusively tailor-made to suit the PET imaging. The agents
124
I is prominently employed in detecting
Cancer Theranostics: Pharmaceutical View
DOI: http://ITexLi.113913
have to facilitate imaging and have suitable pharmacokinetic properties [72]. A
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thorough in vivo validation has to be performed for theranostic PET agents.
Currently, there are multiple theranostic agents being studied at pre-clinical and
clinical levels. Focusing on the recent preclinical development in cancer theranostics,
HER3 overexpression can result in resistance against cancer therapy. Andersson et
developed a radiolabeled anti-HER3 affibody 111In-HEHEHE-Z08698-NOTA which
exhibited impressive affinity towards HER3 receptor [73]. Cobalamin is another
interesting agent currently in preclinical research. Kuda-Wedagedara et
to radiolabel cobalamin and used it in PET imaging [74]. Nanotechnology is a wellestablished drug delivery approach. Despite the advancements, it is surprising that
no nano-theranostic agent has been approved by USFDA to date. This is explained
through translation difficulties existing in preclinical to clinical conversion of nanotheranostics [75].
al. used 89Zr
al
. Theranostics in the market
The success of any therapeutic, diagnostic, or theranostic agent lies in its safety
and efficacy. Despite its attractions, theranostics come with safety concerns due to the
use of radioactive agents. Potential toxicity, incompatibilities, and interactions are to
be established. Nuclear medicines are complex in terms of production, handling, and
administration. Speaking in terms of cost, theranostic agents require special production facilities for handling radioactive, sophisticated instruments, skilled personnel,
and critical training [76]. Launching a new drug into the market is an expensive
licensing process. When it comes to the theranostic agent, the marginal cost multiplies.
Quality and reproducibility must be compliant for each batch. Commercialization also
adds to the cost.
Translating a theranostic agent to clinical use is quite a hurdle. The concept of one
dose is not applicable in theranostics. The patient-dependent tailoring may rise as a
challenge during clinical and regulatory approvals [77].
.,
. Conclusion
Theranostics is a fancy term with enormous potential to serve as a novel approach
to deadly diseases like cancer. It aids in early diagnosis and treatment of silent cancers,
as time is the ultimate. Combining a diagnostic and therapeutic agent minimizes the
cost, duration, and labor in individual therapy. Falling under personalized medicine, theranostics provide patient-tailored drug delivery with specific dosimetry.
Radionuclides provide visibility and promote easy diagnosis of complex tumors.
Speaking beyond the advantages, theranostics is still a questionable approach based
on its safety and efficacy. It is challenging both in terms of production and clinical
setting. We draw a firm conclusion that theranostics is a potential tool in cancer
detection and treatment and it should come with uncompromised safety.
Acknowledgements
The authors are thankful to KMCH College of Pharmacy, Coimbatore, for their
constant support.
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Cancer Theranostics: Pharmaceutical View
DOI: http://ITexLi.113913
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